Photorespiration Is Crucial for Dynamic Response of Photosynthetic Metabolism and Stomatal Movement to Altered CO2 Availability

Eisenhut M, Bräutigam A, Timm S, Florian A, Tohge T, Fernie AR, Bauwe H, Weber APM (2017)
Molecular Plant 10(1): 47-61.

Download
OA 1.88 MB
Zeitschriftenaufsatz | Veröffentlicht | Englisch
Volltext vorhanden für diesen Nachweis
Autor
; ; ; ; ; ; ;
Abstract / Bemerkung
The photorespiratory pathway or photorespiration is an essential process in oxygenic photosynthetic organisms, which can reduce the efficiency of photosynthetic carbon assimilation and is hence frequently considered as a wasteful process. By comparing the response of the wild-type plants and mutants impaired in photorespiration to a shift in ambient CO2 concentrations, we demonstrate that photorespiration also plays a beneficial role during short-term acclimation to reduced CO2 availability. The wild-type plants responded with few differentially expressed genes, mostly involved in drought stress, which is likely a consequence of enhanced opening of stomata and concomitant water loss upon a shift toward low CO2. In contrast, mutants with impaired activity of photorespiratory enzymes were highly stressed and not able to adjust stomatal conductance to reduced external CO2 availability. The transcriptional response of mutant plants was congruent, indicating a general reprogramming to deal with the consequences of reduced CO2 availability, signaled by enhanced oxygenation of ribulose-1,5-bisphosphate and amplified by the artificially impaired photorespiratory metabolism. Central in this reprogramming was the pronounced reallocation of resources from growth processes to stress responses. Taken together, our results indicate that unrestricted photorespiratory metabolism is a prerequisite for rapid physiological acclimation to a reduction in CO2 availability.
Erscheinungsjahr
Zeitschriftentitel
Molecular Plant
Band
10
Ausgabe
1
Seite(n)
47-61
ISSN
eISSN
PUB-ID

Zitieren

Eisenhut M, Bräutigam A, Timm S, et al. Photorespiration Is Crucial for Dynamic Response of Photosynthetic Metabolism and Stomatal Movement to Altered CO2 Availability. Molecular Plant. 2017;10(1):47-61.
Eisenhut, M., Bräutigam, A., Timm, S., Florian, A., Tohge, T., Fernie, A. R., Bauwe, H., et al. (2017). Photorespiration Is Crucial for Dynamic Response of Photosynthetic Metabolism and Stomatal Movement to Altered CO2 Availability. Molecular Plant, 10(1), 47-61. doi:10.1016/j.molp.2016.09.011
Eisenhut, M., Bräutigam, A., Timm, S., Florian, A., Tohge, T., Fernie, A. R., Bauwe, H., and Weber, A. P. M. (2017). Photorespiration Is Crucial for Dynamic Response of Photosynthetic Metabolism and Stomatal Movement to Altered CO2 Availability. Molecular Plant 10, 47-61.
Eisenhut, M., et al., 2017. Photorespiration Is Crucial for Dynamic Response of Photosynthetic Metabolism and Stomatal Movement to Altered CO2 Availability. Molecular Plant, 10(1), p 47-61.
M. Eisenhut, et al., “Photorespiration Is Crucial for Dynamic Response of Photosynthetic Metabolism and Stomatal Movement to Altered CO2 Availability”, Molecular Plant, vol. 10, 2017, pp. 47-61.
Eisenhut, M., Bräutigam, A., Timm, S., Florian, A., Tohge, T., Fernie, A.R., Bauwe, H., Weber, A.P.M.: Photorespiration Is Crucial for Dynamic Response of Photosynthetic Metabolism and Stomatal Movement to Altered CO2 Availability. Molecular Plant. 10, 47-61 (2017).
Eisenhut, Marion, Bräutigam, Andrea, Timm, Stefan, Florian, Alexandra, Tohge, Takayuki, Fernie, Alisdair R., Bauwe, Hermann, and Weber, Andreas P. M. “Photorespiration Is Crucial for Dynamic Response of Photosynthetic Metabolism and Stomatal Movement to Altered CO2 Availability”. Molecular Plant 10.1 (2017): 47-61.
Alle Dateien verfügbar unter der/den folgenden Lizenz(en):
Copyright Statement:
This Item is protected by copyright and/or related rights. [...]
Volltext(e)
Access Level
OA Open Access
Zuletzt Hochgeladen
2017-12-15T10:12:58Z

9 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
Low CO2 induces urea cycle intermediate accumulation in Arabidopsis thaliana.
Blume C, Ost J, Mühlenbruch M, Peterhänsel C, Laxa M., PLoS One 14(1), 2019
PMID: 30650113
Rubisco is not really so bad.
Bathellier C, Tcherkez G, Lorimer GH, Farquhar GD., Plant Cell Environ 41(4), 2018
PMID: 29359811
The Photorespiratory Metabolite 2-Phosphoglycolate Regulates Photosynthesis and Starch Accumulation in Arabidopsis.
Flügel F, Timm S, Arrivault S, Florian A, Stitt M, Fernie AR, Bauwe H., Plant Cell 29(10), 2017
PMID: 28947491

68 References

Daten bereitgestellt von Europe PubMed Central.


Alexa, 2010
Chloroplast and cytoplasmic enzymes. II. Pea leaf triose phosphate isomerases.
Anderson LE., Biochim. Biophys. Acta 235(1), 1971
PMID: 5089710
Identification of the 2-hydroxyglutarate and isovaleryl-CoA dehydrogenases as alternative electron donors linking lysine catabolism to the electron transport chain of Arabidopsis mitochondria.
Araujo WL, Ishizaki K, Nunes-Nesi A, Larson TR, Tohge T, Krahnert I, Witt S, Obata T, Schauer N, Graham IA, Leaver CJ, Fernie AR., Plant Cell 22(5), 2010
PMID: 20501910
Guard cell photosynthesis is critical for stomatal turgor production, yet does not directly mediate CO2 - and ABA-induced stomatal closing.
Azoulay-Shemer T, Palomares A, Bagheri A, Israelsson-Nordstrom M, Engineer CB, Bargmann BO, Stephan AB, Schroeder JI., Plant J. 83(4), 2015
PMID: 26096271
Photorespiration has a dual origin and manifold links to central metabolism.
Bauwe H, Hagemann M, Kern R, Timm S., Curr. Opin. Plant Biol. 15(3), 2012
PMID: 22284850
Controlling the false discovery rate: a practical and powerful approach to multiple testing
Benjamini, J. R. Stat. Soc. B 57(), 1995
D-GLYCERATE 3-KINASE, the last unknown enzyme in the photorespiratory cycle in Arabidopsis, belongs to a novel kinase family.
Boldt R, Edner C, Kolukisaoglu U, Hagemann M, Weckwerth W, Wienkoop S, Morgenthal K, Bauwe H., Plant Cell 17(8), 2005
PMID: 15980259
Growth stage-based phenotypic analysis of Arabidopsis: a model for high throughput functional genomics in plants.
Boyes DC, Zayed AM, Ascenzi R, McCaskill AJ, Hoffman NE, Davis KR, Gorlach J., Plant Cell 13(7), 2001
PMID: 11449047
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
Reversible Burst of Transcriptional Changes during Induction of Crassulacean Acid Metabolism in Talinum triangulare.
Brilhaus D, Brautigam A, Mettler-Altmann T, Winter K, Weber AP., Plant Physiol. 170(1), 2015
PMID: 26530316
WRKY75 transcription factor is a modulator of phosphate acquisition and root development in Arabidopsis.
Devaiah BN, Karthikeyan AS, Raghothama KG., Plant Physiol. 143(4), 2007
PMID: 17322336
Four distinct types of dehydration stress memory genes in Arabidopsis thaliana.
Ding Y, Liu N, Virlouvet L, Riethoven JJ, Fromm M, Avramova Z., BMC Plant Biol. 13(), 2013
PMID: 24377444
The photorespiratory glycolate metabolism is essential for cyanobacteria and might have been conveyed endosymbiontically to plants.
Eisenhut M, Ruth W, Haimovich M, Bauwe H, Kaplan A, Hagemann M., Proc. Natl. Acad. Sci. U.S.A. 105(44), 2008
PMID: 18957552
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
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
The global carbon cycle: a test of our knowledge of earth as a system.
Falkowski P, Scholes RJ, Boyle E, Canadell J, Canfield D, Elser J, Gruber N, Hibbard K, Hogberg P, Linder S, Mackenzie FT, Moore B 3rd, Pedersen T, Rosenthal Y, Seitzinger S, Smetacek V, Steffen W., Science 290(5490), 2000
PMID: 11030643
The bHLH transcription factor HBI1 mediates the trade-off between growth and pathogen-associated molecular pattern-triggered immunity in Arabidopsis.
Fan M, Bai MY, Kim JG, Wang T, Oh E, Chen L, Park CH, Son SH, Kim SK, Mudgett MB, Wang ZY., Plant Cell 26(2), 2014
PMID: 24550223
On the interpretation of χ2 from contingency tables, and the calculation of P
Fisher, J. R. Stat. Soc. 85(), 1922
Dark-inducible genes from Arabidopsis thaliana are associated with leaf senescence and repressed by sugars.
Fujiki Y, Yoshikawa Y, Sato T, Inada N, Ito M, Nishida I, Watanabe A., Physiol Plant 111(3), 2001
PMID: 11240919
Molecular crosstalk between PAMP-triggered immunity and photosynthesis.
Gohre V, Jones AM, Sklenar J, Robatzek S, Weber AP., Mol. Plant Microbe Interact. 25(8), 2012
PMID: 22550958
What is the physiological role of photorespiration?
Heber, Trends Biochem. Sci. 5(), 1980
Protein phosphorylation and photorespiration.
Hodges M, Jossier M, Boex-Fontvieille E, Tcherkez G., Plant Biol (Stuttg) 15(4), 2013
PMID: 23506267
Blue Light Induces a Distinct Starch Degradation Pathway in Guard Cells for Stomatal Opening.
Horrer D, Flutsch S, Pazmino D, Matthews JS, Thalmann M, Nigro A, Leonhardt N, Lawson T, Santelia D., Curr. Biol. 26(3), 2016
PMID: 26774787
Carbonic anhydrases are upstream regulators of CO2-controlled stomatal movements in guard cells.
Hu H, Boisson-Dernier A, Israelsson-Nordstrom M, Bohmer M, Xue S, Ries A, Godoski J, Kuhn JM, Schroeder JI., Nat. Cell Biol. 12(1), 2009
PMID: 20010812
Blue light-induced autophosphorylation of phototropin is a primary step for signaling.
Inoue S, Kinoshita T, Matsumoto M, Nakayama KI, Doi M, Shimazaki K., Proc. Natl. Acad. Sci. U.S.A. 105(14), 2008
PMID: 18378899
The redox control of photorespiration: from biochemical and physiological aspects to biotechnological considerations
Keech, Plant Cell Environ. (), 2016
Inhibition of spinach-leaf phosphofructokinase by 2-phosphoglycollate.
Kelly GJ, Latzko E., FEBS Lett. 68(1), 1976
PMID: 134908
Phot1 and phot2 mediate blue light regulation of stomatal opening.
Kinoshita T, Doi M, Suetsugu N, Kagawa T, Wada M, Shimazaki K., Nature 414(6864), 2001
PMID: 11740564
Closing gaps: linking elements that control stomatal movement.
Kollist H, Nuhkat M, Roelfsema MR., New Phytol. 203(1), 2014
PMID: 24800691
Photorespiration protects C3 plants from photooxidation
Kozaki, Nature 384(), 1996
NADPH oxidase AtrbohD and AtrbohF genes function in ROS-dependent ABA signaling in Arabidopsis.
Kwak JM, Mori IC, Pei ZM, Leonhardt N, Torres MA, Dangl JL, Bloom RE, Bodde S, Jones JD, Schroeder JI., EMBO J. 22(11), 2003
PMID: 12773379
Gas chromatography mass spectrometry-based metabolite profiling in plants.
Lisec J, Schauer N, Kopka J, Willmitzer L, Fernie AR., Nat Protoc 1(1), 2006
PMID: 17406261
Light-induced modification of plant plasma membrane ion transport.
Marten I, Deeken R, Hedrich R, Roelfsema MR., Plant Biol (Stuttg) 12 Suppl 1(), 2010
PMID: 20712622
Disruption of the glycolate dehydrogenase gene in the high-CO₂-requiring mutant HCR89 of Chlamydomonas reinhardtii.
Nakamura Y, Kanakagiri S, Van K, He W, Spalding MH., Can. J. Bot. 83(7), 2005
PMID: IND43761130
The age of Rubisco: the evolution of oxygenic photosynthesis
Nisbet, Geobiology 5(), 2007
Photorespiration and photoinhibition. Some implications for the energetics of photosynthesis
Osmond, Biochim. Biophys. Acta 639(), 1981
ABR1, an APETALA2-domain transcription factor that functions as a repressor of ABA response in Arabidopsis.
Pandey GK, Grant JJ, Cheong YH, Kim BG, Li L, Luan S., Plant Physiol. 139(3), 2005
PMID: 16227468
PLGG1, a plastidic glycolate glycerate transporter, is required for photorespiration and defines a unique class of metabolite transporters.
Pick TR, Brautigam A, Schulz MA, Obata T, Fernie AR, Weber AP., Proc. Natl. Acad. Sci. U.S.A. 110(8), 2013
PMID: 23382251
ß-amylase1 mutant Arabidopsis plants show improved drought tolerance due to reduced starch breakdown in guard cells.
Prasch CM, Ott KV, Bauer H, Ache P, Hedrich R, Sonnewald U., J. Exp. Bot. 66(19), 2015
PMID: 26139825
Day length is a key regulator of transcriptomic responses to both CO(2) and H(2)O(2) in Arabidopsis.
Queval G, Neukermans J, Vanderauwera S, Van Breusegem F, Noctor G., Plant Cell Environ. 35(2), 2011
PMID: 21631535
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
Strategies to maintain redox homeostasis during photosynthesis under changing conditions.
Scheibe R, Backhausen JE, Emmerlich V, Holtgrefe S., J. Exp. Bot. 56(416), 2005
PMID: 15851411
Light regulation of stomatal movement.
Shimazaki K, Doi M, Assmann SM, Kinoshita T., Annu Rev Plant Biol 58(), 2007
PMID: 17209798
A phosphoglycolate phosphatase-deficient mutant of Arabidopsis
Somerville, Nature 280(), 1979
The Arabidopsis Information Resource (TAIR): gene structure and function annotation.
Swarbreck D, Wilks C, Lamesch P, Berardini TZ, Garcia-Hernandez M, Foerster H, Li D, Meyer T, Muller R, Ploetz L, Radenbaugh A, Singh S, Swing V, Tissier C, Zhang P, Huala E., Nucleic Acids Res. 36(Database issue), 2007
PMID: 17986450
Metabolic fluxes in an illuminated Arabidopsis rosette.
Szecowka M, Heise R, Tohge T, Nunes-Nesi A, Vosloh D, Huege J, Feil R, Lunn J, Nikoloski Z, Stitt M, Fernie AR, Arrivault S., Plant Cell 25(2), 2013
PMID: 23444331
Photoprotection in plants: a new light on photosystem II damage.
Takahashi S, Badger MR., Trends Plant Sci. 16(1), 2010
PMID: 21050798
A molecular pathway for CO₂ response in Arabidopsis guard cells.
Tian W, Hou C, Ren Z, Pan Y, Jia J, Zhang H, Bai F, Zhang P, Zhu H, He Y, Luo S, Li L, Luan S., Nat Commun 6(), 2015
PMID: 25599916
A cytosolic pathway for the conversion of hydroxypyruvate to glycerate during photorespiration in Arabidopsis.
Timm S, Nunes-Nesi A, Parnik T, Morgenthal K, Wienkoop S, Keerberg O, Weckwerth W, Kleczkowski LA, Fernie AR, Bauwe H., Plant Cell 20(10), 2008
PMID: 18952776
The hydroxypyruvate-reducing system in Arabidopsis: multiple enzymes for the same end.
Timm S, Florian A, Jahnke K, Nunes-Nesi A, Fernie AR, Bauwe H., Plant Physiol. 155(2), 2010
PMID: 21205613
High-to-low CO2 acclimation reveals plasticity of the photorespiratory pathway and indicates regulatory links to cellular metabolism of Arabidopsis.
Timm S, Mielewczik M, Florian A, Frankenbach S, Dreissen A, Hocken N, Fernie AR, Walter A, Bauwe H., PLoS ONE 7(8), 2012
PMID: 22912743
Perturbation of indole-3-butyric acid homeostasis by the UDP-glucosyltransferase UGT74E2 modulates Arabidopsis architecture and water stress tolerance.
Tognetti VB, Van Aken O, Morreel K, Vandenbroucke K, van de Cotte B, De Clercq I, Chiwocha S, Fenske R, Prinsen E, Boerjan W, Genty B, Stubbs KA, Inze D, Van Breusegem F., Plant Cell 22(8), 2010
PMID: 20798329
The photorespiratory Arabidopsis shm1 mutant is deficient in SHM1.
Voll LM, Jamai A, Renne P, Voll H, McClung CR, Weber AP., Plant Physiol. 140(1), 2005
PMID: 16339799
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
Carbon balance and circadian regulation of hydrolytic and phosphorolytic breakdown of transitory starch.
Weise SE, Schrader SM, Kleinbeck KR, Sharkey TD., Plant Physiol. 141(3), 2006
PMID: 16698896
The Arabidopsis AP2/ERF transcription factor RAP2.6 participates in ABA, salt and osmotic stress responses.
Zhu Q, Zhang J, Gao X, Tong J, Xiao L, Li W, Zhang H., Gene 457(1-2), 2010
PMID: 20193749

Export

Markieren/ Markierung löschen
Markierte Publikationen

Open Data PUB

Web of Science

Dieser Datensatz im Web of Science®

Quellen

PMID: 27702693
PubMed | Europe PMC

Suchen in

Google Scholar