Most photorespiratory genes are preferentially expressed in the bundle sheath cells of the C-4 grass Sorghum bicolor

Döring F, Streubel M, Bräutigam A, Gowik U (2016)
Journal of Experimental Botany 67(10): 3053-3064.

Zeitschriftenaufsatz | Veröffentlicht | Englisch
OA 6.23 MB
Döring, Florian; Streubel, Monika; Bräutigam, AndreaUniBi ; Gowik, Udo
Abstract / Bemerkung
Photorespiratory genes are expressed tissue-specific in the leaves of the C-4 grass Sorghum bicolor. Most but not all of them are confined to the bundle sheath cells.One of the hallmarks of C-4 plants is the division of labor between two different photosynthetic cell types, the mesophyll and the bundle sheath cells. C-4 plants are of polyphyletic origin and, during the evolution of C-4 photosynthesis, the expression of thousands of genes was altered and many genes acquired a cell type-specific or preferential expression pattern. Several lines of evidence, including computational modeling and physiological and phylogenetic analyses, indicate that alterations in the expression of a key photorespiration-related gene, encoding the glycine decarboxylase P subunit, was an early and important step during C-4 evolution. Restricting the expression of this gene to the bundle sheath led to the establishment of a photorespiratory CO2 pump. We were interested in whether the expression of genes related to photorespiration remains bundle sheath specific in a fully optimized C-4 species. Therefore we analyzed the expression of photorespiratory and C-4 cycle genes using RNA in situ hybridization and transcriptome analysis of isolated mesophyll and bundle sheath cells in the C-4 grass Sorghum bicolor. It turns out that the C-4 metabolism of Sorghum is based solely on the NADP-dependent malic enzyme pathway. The majority of photorespiratory gene expression, with some important exceptions, is restricted to the bundle sheath.
C-4 photosynthesis; CO2 fixation; differential gene expression; evolution; photorespiration; Sorghum bicolor
Journal of Experimental Botany
Page URI


Döring F, Streubel M, Bräutigam A, Gowik U. Most photorespiratory genes are preferentially expressed in the bundle sheath cells of the C-4 grass Sorghum bicolor. Journal of Experimental Botany. 2016;67(10):3053-3064.
Döring, F., Streubel, M., Bräutigam, A., & Gowik, U. (2016). Most photorespiratory genes are preferentially expressed in the bundle sheath cells of the C-4 grass Sorghum bicolor. Journal of Experimental Botany, 67(10), 3053-3064. doi:10.1093/jxb/erw041
Döring, Florian, Streubel, Monika, Bräutigam, Andrea, and Gowik, Udo. 2016. “Most photorespiratory genes are preferentially expressed in the bundle sheath cells of the C-4 grass Sorghum bicolor”. Journal of Experimental Botany 67 (10): 3053-3064.
Döring, F., Streubel, M., Bräutigam, A., and Gowik, U. (2016). Most photorespiratory genes are preferentially expressed in the bundle sheath cells of the C-4 grass Sorghum bicolor. Journal of Experimental Botany 67, 3053-3064.
Döring, F., et al., 2016. Most photorespiratory genes are preferentially expressed in the bundle sheath cells of the C-4 grass Sorghum bicolor. Journal of Experimental Botany, 67(10), p 3053-3064.
F. Döring, et al., “Most photorespiratory genes are preferentially expressed in the bundle sheath cells of the C-4 grass Sorghum bicolor”, Journal of Experimental Botany, vol. 67, 2016, pp. 3053-3064.
Döring, F., Streubel, M., Bräutigam, A., Gowik, U.: Most photorespiratory genes are preferentially expressed in the bundle sheath cells of the C-4 grass Sorghum bicolor. Journal of Experimental Botany. 67, 3053-3064 (2016).
Döring, Florian, Streubel, Monika, Bräutigam, Andrea, and Gowik, Udo. “Most photorespiratory genes are preferentially expressed in the bundle sheath cells of the C-4 grass Sorghum bicolor”. Journal of Experimental Botany 67.10 (2016): 3053-3064.
Alle Dateien verfügbar unter der/den folgenden Lizenz(en):
Copyright Statement:
Dieses Objekt ist durch das Urheberrecht und/oder verwandte Schutzrechte geschützt. [...]
Access Level
OA Open Access
Zuletzt Hochgeladen
MD5 Prüfsumme

6 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
Efficient 2-phosphoglycolate degradation is required to maintain carbon assimilation and allocation in the C4 plant Flaveria bidentis.
Levey M, Timm S, Mettler-Altmann T, Luca Borghi G, Koczor M, Arrivault S, Pm Weber A, Bauwe H, Gowik U, Westhoff P., J Exp Bot 70(2), 2019
PMID: 30357386
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
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
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

70 References

Daten bereitgestellt von Europe PubMed Central.

Basic local alignment search tool.
Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ., J. Mol. Biol. 215(3), 1990
PMID: 2231712
Chloroplast and cytoplasmic enzymes. II. Pea leaf triose phosphate isomerases.
Anderson LE., Biochim. Biophys. Acta 235(1), 1971
PMID: 5089710
Two different mechanisms for transport of pyruvate into mesophyll chloroplasts of C plants—a comparative study
Aoki N, Ohnishi J, Kanai R., 1992
Photorespiration: players, partners and origin.
Bauwe H, Hagemann M, Fernie AR., Trends Plant Sci. 15(6), 2010
PMID: 20403720
Photorespiration: the bridge to C4 photosynthesis
Bauwe H., 2011
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
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
Leaf structure and development in C4 plants
Dengler NG, Nelson T., 1999
Identification of Photosynthesis-Associated C4 Candidate Genes through Comparative Leaf Gradient Transcriptome in Multiple Lineages of C3 and C4 Species.
Ding Z, Weissmann S, Wang M, Du B, Huang L, Wang L, Tu X, Zhong S, Myers C, Brutnell TP, Sun Q, Li P., PLoS ONE 10(10), 2015
PMID: 26465154
Arabidopsis A BOUT DE SOUFFLE is a putative mitochondrial transporter involved in photorespiratory metabolism and is required for meristem growth at ambient CO₂ levels.
Eisenhut M, Planchais S, Cabassa C, Guivarc'h A, Justin AM, Taconnat L, Renou JP, Linka M, Gagneul D, Timm S, Bauwe H, Carol P, Weber AP., Plant J. 73(5), 2013
PMID: 23181524
Perspectives on plant photorespiratory metabolism.
Fernie AR, Bauwe H, Eisenhut M, Florian A, Hanson DT, Hagemann M, Keech O, Mielewczik M, Nikoloski Z, Peterhansel C, Roje S, Sage R, Timm S, von Cammerer S, Weber AP, Westhoff P., Plant Biol (Stuttg) 15(4), 2012
PMID: 23231538
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
The localization of serine hydroxymethyltransferase in leaves of C3 and C4 species
Gardeström P, Edwards GE, Henricson D, Ericson I., 1985
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

Haberlandt G., 1904
C4 photosynthesis: a unique blend of modified biochemistry, anatomy and ultrastructure
Hatch MD., 1987
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
Glycine decarboxylase is confined to the bundle-sheath cells of leaves of C3-C 4 intermediate species.
Hylton CM, Rawsthorne S, Smith AM, Jones DA, Woolhouse HW., Planta 175(4), 1988
PMID: 24221925
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
C2 photosynthesis generates about 3-fold elevated leaf CO2 levels in the C3-C4 intermediate species Flaveria pubescens.
Keerberg O, Parnik T, Ivanova H, Bassuner B, Bauwe H., J. Exp. Bot. 65(13), 2014
PMID: 24916069
The chloroplastic 2-oxoglutarate/malate transporter has dual function as the malate valve and in carbon/nitrogen metabolism.
Kinoshita H, Nagasaki J, Yoshikawa N, Yamamoto A, Takito S, Kawasaki M, Sugiyama T, Miyake H, Weber APM, Taniguchi M., Plant J. 65(1), 2010
PMID: 21175886
Differential expression of plastome-encoded ndh genes in mesophyll and bundle-sheath chloroplasts of the C4 plant Sorghum bicolor indicates that the complex I-homologous NAD(P)H-plastoquinone oxidoreductase is involved in cyclic electron transport
Kubicki A, Funk E, Westhoff P, Steinmüller K., 1996
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
C4 syndrome—structural-analysis
Laetsch WM., 1974
Ultrafast and memory-efficient alignment of short DNA sequences to the human genome.
Langmead B, Trapnell C, Pop M, Salzberg SL., Genome Biol. 10(3), 2009
PMID: 19261174
The developmental dynamics of the maize leaf transcriptome.
Li P, Ponnala L, Gandotra N, Wang L, Si Y, Tausta SL, Kebrom TH, Provart N, Patel R, Myers CR, Reidel EJ, Turgeon R, Liu P, Sun Q, Nelson T, Brutnell TP., Nat. Genet. 42(12), 2010
PMID: 21037569
Environmental responses
Long SP., 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 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
Why are the 2-oxoacid dehydrogenase complexes so large? Generation of an active trimeric complex.
Marrott NL, Marshall JJ, Svergun DI, Crennell SJ, Hough DW, van den Elsen JM, Danson MJ., Biochem. J. 463(3), 2014
PMID: 25088564
Gene expression analysis of plant host–pathogen interactions by SuperSAGE
Matsumura H, Reich S, Ito A, Saitoh H, Kamoun S, Winter P, Kahl G, Reuter M, Kruger DH, Terauchi R., 2003
The roles of malate and aspartate in C4 photosynthetic metabolism of Flaveria bidentis (L.)
Meister M, Agostino A, Hatch MD., 1996
Coordination of the cell-specific distribution of the four subunits of glycine decarboxylase and of serine hydroxymethyltransferase in leaves of C3–C4 intermediate species from different genera
Morgan CL, Turner SR, Rawsthorne S., 1993
Efficiency of Nitrogen Utilization in C3 and C4 Cereals.
Oaks A., Plant Physiol. 106(2), 1994
PMID: 12232337
Photorespiration: pathways, regulation, and modification
Ogren WL., 1984
Differentiation of photorespiratory activity between mesophyll and bundle sheath cells of C4 plants I. Glycine oxidation by mitochondria
Ohnishi J-i, Kanai R., 1983
Differentiation of photorespiratory activity between mesophyll and bundle sheath cells of C4 plants II. Peroxisomes of Panicum miliaceum L
Ohnishi J-i, Yamazaki M, Kanai R., 1985
Ecological selection pressures for C4 photosynthesis in the grasses.
Osborne CP, Freckleton RP., Proc. Biol. Sci. 276(1663), 2009
PMID: 19324795
The Sorghum bicolor genome and the diversification of grasses.
Paterson AH, Bowers JE, Bruggmann R, Dubchak I, Grimwood J, Gundlach H, Haberer G, Hellsten U, Mitros T, Poliakov A, Schmutz J, Spannagl M, Tang H, Wang X, Wicker T, Bharti AK, Chapman J, Feltus FA, Gowik U, Grigoriev IV, Lyons E, Maher CA, Martis M, Narechania A, Otillar RP, Penning BW, Salamov AA, Wang Y, Zhang L, Carpita NC, Freeling M, Gingle AR, Hash CT, Keller B, Klein P, Kresovich S, McCann MC, Ming R, Peterson DG, Mehboob-ur-Rahman , Ware D, Westhoff P, Mayer KF, Messing J, Rokhsar DS., Nature 457(7229), 2009
PMID: 19189423
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
PLGG1, a plastidic glycolate glycerate transporter, is required for photorespiration and defines a unique class of metabolite transporters
Pick TR, Bräutigam A, Schulz MA, Obata T, Fernie AR, Weber AP., 2013
The Arabidopsis mutant dct is deficient in the plastidic glutamate/malate translocator DiT2.
Renne P, Dressen U, Hebbeker U, Hille D, Flugge UI, Westhoff P, Weber AP., Plant J. 35(3), 2003
PMID: 12887583
The evolution of C4 photosynthesis
Sage RF., 2004
The C(4) plant lineages of planet Earth.
Sage RF, Christin PA, Edwards EJ., J. Exp. Bot. 62(9), 2011
PMID: 21414957
Photorespiration and the evolution of C4 photosynthesis.
Sage RF, Sage TL, Kocacinar F., Annu Rev Plant Biol 63(), 2012
PMID: 22404472
A multi-treatment experimental system to examine photosynthetic differentiation in the maize leaf.
Sawers RJ, Liu P, Anufrikova K, Hwang JT, Brutnell TP., BMC Genomics 8(), 2007
PMID: 17212830
Molecular and biochemical analysis of Arabidopsis
Simon R., 2002
Developmental dynamics of Kranz cell transcriptional specificity in maize leaf reveals early onset of C4-related processes.
Tausta SL, Li P, Si Y, Gandotra N, Liu P, Sun Q, Brutnell TP, Nelson T., J. Exp. Bot. 65(13), 2014
PMID: 24790109
DEGseq: an R package for identifying differentially expressed genes from RNA-seq data.
Wang L, Feng Z, Wang X, Wang X, Zhang X., Bioinformatics 26(1), 2009
PMID: 19855105
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
Comparative genomic analysis of C4 photosynthetic pathway evolution in grasses.
Wang X, Gowik U, Tang H, Bowers JE, Westhoff P, Paterson AH., Genome Biol. 10(6), 2009
PMID: 19549309
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
Plastid transport and metabolism of C3 and C4 plants—comparative analysis and possible biotechnological exploitation
Weber AP, von S., 2010
Phenotypic landscape inference reveals multiple evolutionary paths to C4 photosynthesis.
Williams BP, Johnston IG, Covshoff S, Hibberd JM., Elife 2(), 2013
PMID: 24082995
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
Deficient photosystem II in agranal bundle sheath chloroplasts of C4 plants
Woo KC, Anderson JM, Boardman NK, Downton WJ, Osmond CB, Thorne SW., 1970
The molecular basis of C4 photosynthesis in sorghum: isolation, characterization and RFLP mapping of mesophyll- and bundle-sheath-specific cDNAs obtained by differential screening.
Wyrich R, Dressen U, Brockmann S, Streubel M, Chang C, Qiang D, Paterson AH, Westhoff P., Plant Mol. Biol. 37(2), 1998
PMID: 9617804
High glycolate oxidase activity is required for survival of maize in normal air.
Zelitch I, Schultes NP, Peterson RB, Brown P, Brutnell TP., Plant Physiol. 149(1), 2008
PMID: 18805949

Markieren/ Markierung löschen
Markierte Publikationen

Open Data PUB

Web of Science

Dieser Datensatz im Web of Science®

PMID: 26976818
PubMed | Europe PMC

Suchen in

Google Scholar