Photosynthesis in C-3-C-4 intermediate Moricandia species

Schlueter U, Bräutigam A, Gowik U, Melzer M, Christin P-A, Kurz S, Mettler-Altmann T, Weber APM (2017)
Journal of Experimental Botany 68(2): 191-206.

Zeitschriftenaufsatz | Veröffentlicht | Englisch
 
Download
OA 10.18 MB
Autor*in
Schlueter, Urte; Bräutigam, AndreaUniBi ; Gowik, Udo; Melzer, Michael; Christin, Pascal-Antoine; Kurz, Samantha; Mettler-Altmann, Tabea; Weber, Andreas P. M.
Abstract / Bemerkung
Evolution of C-4 photosynthesis is not distributed evenly in the plant kingdom. Particularly interesting is the situation in the Brassicaceae, because the family contains no C-4 species, but several C-3-C-4 intermediates, mainly in the genus Moricandia. Investigation of leaf anatomy, gas exchange parameters, the metabolome, and the transcriptome of two C-3-C-4 intermediate Moricandia species, M. arvensis and M. suffruticosa, and their close C-3 relative M. moricandioides enabled us to unravel the specific C-3-C-4 characteristics in these Moricandia lines. Reduced CO2 compensation points in these lines were accompanied by anatomical adjustments, such as centripetal concentration of organelles in the bundle sheath, and metabolic adjustments, such as the balancing of C and N metabolism between mesophyll and bundle sheath cells by multiple pathways. Evolution from C-3 to C-3-C-4 intermediacy was probably facilitated first by loss of one copy of the glycine decarboxylase P-protein, followed by dominant activity of a bundle sheath-specific element in its promoter. In contrast to recent models, installation of the C-3-C-4 pathway was not accompanied by enhanced activity of the C-4 cycle. Our results indicate that metabolic limitations connected to N metabolism or anatomical limitations connected to vein density could have constrained evolution of C-4 in Moricandia.
Stichworte
Bundle sheath; C-3-C-4 intermediacy; C-4 photosynthesis; evolution; glycine decarboxylase; Moricandia
Erscheinungsjahr
2017
Zeitschriftentitel
Journal of Experimental Botany
Band
68
Ausgabe
2
Seite(n)
191-206
ISSN
0022-0957
eISSN
1460-2431
Page URI
https://pub.uni-bielefeld.de/record/2915125

Zitieren

Schlueter U, Bräutigam A, Gowik U, et al. Photosynthesis in C-3-C-4 intermediate Moricandia species. Journal of Experimental Botany. 2017;68(2):191-206.
Schlueter, U., Bräutigam, A., Gowik, U., Melzer, M., Christin, P. - A., Kurz, S., Mettler-Altmann, T., et al. (2017). Photosynthesis in C-3-C-4 intermediate Moricandia species. Journal of Experimental Botany, 68(2), 191-206. doi:10.1093/jxb/erw391
Schlueter, Urte, Bräutigam, Andrea, Gowik, Udo, Melzer, Michael, Christin, Pascal-Antoine, Kurz, Samantha, Mettler-Altmann, Tabea, and Weber, Andreas P. M. 2017. “Photosynthesis in C-3-C-4 intermediate Moricandia species”. Journal of Experimental Botany 68 (2): 191-206.
Schlueter, U., Bräutigam, A., Gowik, U., Melzer, M., Christin, P. - A., Kurz, S., Mettler-Altmann, T., and Weber, A. P. M. (2017). Photosynthesis in C-3-C-4 intermediate Moricandia species. Journal of Experimental Botany 68, 191-206.
Schlueter, U., et al., 2017. Photosynthesis in C-3-C-4 intermediate Moricandia species. Journal of Experimental Botany, 68(2), p 191-206.
U. Schlueter, et al., “Photosynthesis in C-3-C-4 intermediate Moricandia species”, Journal of Experimental Botany, vol. 68, 2017, pp. 191-206.
Schlueter, U., Bräutigam, A., Gowik, U., Melzer, M., Christin, P.-A., Kurz, S., Mettler-Altmann, T., Weber, A.P.M.: Photosynthesis in C-3-C-4 intermediate Moricandia species. Journal of Experimental Botany. 68, 191-206 (2017).
Schlueter, Urte, Bräutigam, Andrea, Gowik, Udo, Melzer, Michael, Christin, Pascal-Antoine, Kurz, Samantha, Mettler-Altmann, Tabea, and Weber, Andreas P. M. “Photosynthesis in C-3-C-4 intermediate Moricandia species”. Journal of Experimental Botany 68.2 (2017): 191-206.
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
0ec1ea3f93da93bdba1de9169011326b


5 Zitationen in Europe PMC

Daten bereitgestellt von Europe PubMed Central.

Metabolic regulation of photosynthesis.
Heyneke E, Fernie AR., Biochem Soc Trans 46(2), 2018
PMID: 29523770
Reactive oxygen species and redox regulation in mesophyll and bundle sheath cells of C4 plants.
Turkan I, Uzilday B, Dietz KJ, Bräutigam A, Ozgur R., J Exp Bot 69(14), 2018
PMID: 29529246
C4 photosynthesis: 50 years of discovery and innovation.
von Caemmerer S, Ghannoum O, Furbank RT., J Exp Bot 68(2), 2017
PMID: 28110274
Molecular phylogeny and evolutionary history of Moricandia DC (Brassicaceae).
Perfectti F, Gómez JM, González-Megías A, Abdelaziz M, Lorite J., PeerJ 5(), 2017
PMID: 29093999
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

80 References

Daten bereitgestellt von Europe PubMed Central.

The Moricandia syndrome in species of the Brassicaceae – evolutionary aspects
Apel P, Horstmann C, Pfeffer M., 1997
Diversification times among Brassica (Brassicaceae) crops suggest hybrid formation after 20 million years of divergence.
Arias T, Beilstein MA, Tang M, McKain MR, Pires JC., Am. J. Bot. 101(1), 2014
PMID: 24388963
The enzymes in C photosynthesis
Ashton AR, Burnell JN, Furbank RT, Jenkins CLD, Hatch MD., 1990
The role of proteins in C plants prior to their recruitment into the C pathway
Aubry S, Brown NJ, Hibberd JM., 2011
Biochemical characterization of Moricandia arvensis (L.) DC., a species with features intermediate between C and C photosynthesis, in comparison with the C species Moricandia foetida Bourg
Bauwe H, Apel P., 1979
Trimmomatic: a flexible trimmer for Illumina sequence data.
Bolger AM, Lohse M, Usadel B., Bioinformatics 30(15), 2014
PMID: 24695404
Phosphoglycolate production catalyzed by ribulose diphosphate carboxylase.
Bowes G, Ogren WL, Hageman RH., Biochem. Biophys. Res. Commun. 45(3), 1971
PMID: 4331471
Photorespiration connects C and C photosynthesis
Brautigam A, Gowik U., 2016
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
Towards an integrative model of C photosynthetic subtypes: insights from comparative transcriptome analysis of NAD-ME, NADP-ME, and PEP-CK C species
Brautigam A, Schliesky S, Kulahoglu C, Osborne CP, Weber AP., 2014
Leaf anatomy of c(3)-c(4) species as related to evolution of c(4) photosynthesis.
Brown RH, Hattersley PW., Plant Physiol. 91(4), 1989
PMID: 16667214
Anatomical enablers and the evolution of C photosynthesis in grasses
Christin PA, Osborne CP, Chatelet DS, Columbus JT, Besnard G, Hodkinson TR, Garrison LM, Vorontsova MS, Edwards EJ., 2013
C eudicots are not younger than C monocots
Christin PA, Osborne CP, Sage RF, Arakaki M, Edwards EJ., 2011
Complex evolutionary transitions and the significance of c(3)-c(4) intermediate forms of photosynthesis in Molluginaceae.
Christin PA, Sage TL, Edwards EJ, Ogburn RM, Khoshravesh R, Sage RF., Evolution 65(3), 2010
PMID: 20955197
Molecular dating, evolutionary rates, and the age of the grasses.
Christin PA, Spriggs E, Osborne CP, Stromberg CA, Salamin N, Edwards EJ., Syst. Biol. 63(2), 2013
PMID: 24287097
Quantitative leaf anatomy of C and C grasses (Poaceae): bundle sheath and mesophyll surface area relationships
Dengler NG, Dengler RE, Donnelly PM, Hattersley PW., 1994
BEAST: Bayesian evolutionary analysis by sampling trees.
Drummond AJ, Rambaut A., BMC Evol. Biol. 7(), 2007
PMID: 17996036
agriGO: a GO analysis toolkit for the agricultural community.
Du Z, Zhou X, Ling Y, Zhang Z, Su Z., Nucleic Acids Res. 38(Web Server issue), 2010
PMID: 20435677
Deletion of glycine decarboxylase in Arabidopsis is lethal under nonphotorespiratory conditions.
Engel N, van den Daele K, Kolukisaoglu U, Morgenthal K, Weckwerth W, Parnik T, Keerberg O, Bauwe H., Plant Physiol. 144(3), 2007
PMID: 17496108
Metabolite profiling for plant functional genomics.
Fiehn O, Kopka J, Dormann P, Altmann T, Trethewey RN, Willmitzer L., Nat. Biotechnol. 18(11), 2000
PMID: 11062433
Evolutionary history of Blepharis (Acanthaceae) and the origin of C photosynthesis in section Acanthodium
Fisher AE, McDade LA, Kiel CA, Khoshravesh R, Johnson MA, Stata M, Sage TL, Sage RF., 2015
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
C photosynthesis: a unique blend of modified biochemistry, anatomy and ultrastructure
Hatch MD., 1987
Photosynthetic CO-fixation pathways
Hatch MD, Slack CR., 1970
C4 photosynthesis evolution: the conditional Mt. Fuji.
Heckmann D., Curr. Opin. Plant Biol. 31(), 2016
PMID: 27153468
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
Photosynthetic/photorespiratory CO exchange characteristics of the C-C intermediate species, Moricandia arvensis
Holaday AS, Harrison AT, Chollet R., 1982
Anatomical, ultrastructural and enzymatic studies of leaves of Moricandia arvensis, a C-C intermediate species
Holaday AS, Shien Y-J, Lee KW, Chollet R., 1981
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
Plant species intermediate for c3, c4 photosynthesis.
Kennedy RA, Laetsch WM., Science 184(4141), 1974
PMID: 17736195
BLAT--the BLAST-like alignment tool.
Kent WJ., Genome Res. 12(4), 2002
PMID: 11932250
C-C intermediacy in grasses: organelle enrichment and distribution, glycine decarboxylase expression, and the rise of C photosynthesis
Khoshravesh R, Stinson CR, Stata M, Busch FA, Sage RF, Ludwig M, Sage TL., 2016
Paradigm shift in plant growth control.
Korner C., Curr. Opin. Plant Biol. 25(), 2015
PMID: 26037389
Carbon dioxide compensation points of flowering plants.
Krenzer EG, Moss DN, Crookston RK., Plant Physiol. 56(2), 1975
PMID: 16659272
RNA-Seq based phylogeny recapitulates previous phylogeny of the genus Flaveria (Asteraceae) with some modifications.
Lyu MJ, Gowik U, Kelly S, Covshoff S, Mallmann J, Westhoff P, Hibberd JM, Stata M, Sage RF, Lu H, Wei X, Wong GK, Zhu XG., BMC Evol. Biol. 15(), 2015
PMID: 26084484
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
Phylogeny of Flaveria (Asteraceae) and inference of C4 photosynthesis evolution.
McKown AD, Moncalvo JM, Dengler NG., Am. J. Bot. 92(11), 2005
PMID: 21646108
Nucleotide Metabolism in Salt-Stressed Zea mays L. Root Tips: I. Adenine and Uridine Nucleotides.
Peterson TA, Nieman RH, Clark RA., Plant Physiol. 85(4), 1987
PMID: 16665842
Coordination of the cell-specific distribution of the four subunits of glycine decarboxylase and serine hydroxymethyltransferase in leaves of C–C intermediate species from different genera
Morgan CL, Turner SR, Rawsthorne S., 1993
The origins of Arabidopsis suecica (Brassicaceae) as indicated by nuclear rDNA sequences.
O'Kane SLJr, Schaal BA, Al-Shehbaz IA., Syst. Bot. 21(4), 1996
PMID: IND20601858
Evolution of C plants: a new hypothesis for an interaction of CO and water relations mediated by plant hydraulics
Osborne CP, Sack L., 2012
Greater efficiency of photosynthetic carbon fixation due to single amino-acid substitution
Paulus JK, Schlieper D, Groth G., 2013
C-C intermediate photosynthesis: linking physiology to gene expression
Rawsthorne S., 1992
edgeR: a Bioconductor package for differential expression analysis of digital gene expression data.
Robinson MD, McCarthy DJ, Smyth GK., Bioinformatics 26(1), 2009
PMID: 19910308
The evolution of C 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
From proto-Kranz to C4 Kranz: building the bridge to C4 photosynthesis.
Sage RF, Khoshravesh R, Sage TL., J. Exp. Bot. 65(13), 2014
PMID: 24803502
Photorespiration and the evolution of C4 photosynthesis.
Sage RF, Sage TL, Kocacinar F., Annu Rev Plant Biol 63(), 2012
PMID: 22404472
The occurrence of C(2) photosynthesis in Euphorbia subgenus Chamaesyce (Euphorbiaceae).
Sage TL, Sage RF, Vogan PJ, Rahman B, Johnson DC, Oakley JC, Heckel MA., J. Exp. Bot. 62(9), 2011
PMID: 21459765
The Road to C4 Photosynthesis: Evolution of a Complex Trait via Intermediary States.
Schluter U, Weber AP., Plant Cell Physiol. 57(5), 2016
PMID: 26893471
Evolution of C4 photosynthesis in the genus flaveria: establishment of a photorespiratory CO2 pump.
Schulze S, Mallmann J, Burscheidt J, Koczor M, Streubel M, Bauwe H, Gowik U, Westhoff P., Plant Cell 25(7), 2013
PMID: 23847152
Moricandia
Tahir M, Watts R., 2010

von S., 2000
Emerging concept for the role of photorespiration as an important part of abiotic stress response.
Voss I, Sunil B, Scheibe R, Raghavendra AS., Plant Biol (Stuttg) 15(4), 2013
PMID: 23452019
Phylogeny of tribe Brassiceae (Brassicaceae) based on chloroplast restriction site polymorphisms and nuclear ribosomal internal transcribed spacer and chloroplast trnL intron sequences
Warwick SI, Sauder CA., 2005
Salsola laricifolia, another C-C intermediate species in tribe Salsoleae s.l. (Chenopodiaceae)
Wen Z, Zhang M., 2015
Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics
White TJ, Bruns T, Lee S, Taylor J., 1990
Phenotypic landscape inference reveals multiple evolutionary paths to C4 photosynthesis.
Williams BP, Johnston IG, Covshoff S, Hibberd JM., Elife 2(), 2013
PMID: 24082995
A dominant gdcP-specific marker derived from Moricandia nitens used for introducing the C-C character from M. nitens into Brassica crops
Zhang C, Xu G, Huang R, Chen C, Meng J., 2004
Export

Markieren/ Markierung löschen
Markierte Publikationen

Open Data PUB

Web of Science

Dieser Datensatz im Web of Science®
Quellen

PMID: 28110276
PubMed | Europe PMC

Suchen in

Google Scholar