Reversible Burst of Transcriptional Changes during Induction of Crassulacean Acid Metabolism in Talinum triangulare

Brilhaus D, Bräutigam A, Mettler-Altmann T, Winter K, Weber APM (2016)
Plant Physiology 170(1): 102-122.

Zeitschriftenaufsatz | Veröffentlicht | Englisch
 
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Brilhaus, Dominik; Bräutigam, AndreaUniBi ; Mettler-Altmann, Tabea; Winter, Klaus; Weber, Andreas P. M.
Abstract / Bemerkung
Drought tolerance is a key factor for agriculture in the 21st century as it is a major determinant of plant survival in natural ecosystems as well as crop productivity. Plants have evolved a range of mechanisms to cope with drought, including a specialized type of photosynthesis termed Crassulacean acid metabolism(CAM). CAM is associated with stomatal closure during the day as atmospheric CO2 is assimilated primarily during the night, thus reducing transpirational water loss. The tropical herbaceous perennial species Talinum triangulare is capable of transitioning, in a facultative, reversible manner, from C-3 photosynthesis to weakly expressed CAM in response to drought stress. The transcriptional regulation of this transition has been studied. Combining mRNA-Seq with targeted metabolite measurements, we found highly elevated levels of CAM-cycle enzyme transcripts and their metabolic products in T. triangulare leaves upon water deprivation. The carbohydrate metabolism is rewired to reduce the use of reserves for growth to support the CAM-cycle and the synthesis of compatible solutes. This large-scale expression dataset of drought-induced CAM demonstrates transcriptional regulation of the C-3-CAM transition. We identified candidate transcription factors to mediate this photosynthetic plasticity, which may contribute in the future to the design of more drought-tolerant crops via engineered CAM.
Erscheinungsjahr
2016
Zeitschriftentitel
Plant Physiology
Band
170
Ausgabe
1
Seite(n)
102-122
ISSN
0032-0889
eISSN
1532-2548
Page URI
https://pub.uni-bielefeld.de/record/2915132

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Brilhaus D, Bräutigam A, Mettler-Altmann T, Winter K, Weber APM. Reversible Burst of Transcriptional Changes during Induction of Crassulacean Acid Metabolism in Talinum triangulare. Plant Physiology. 2016;170(1):102-122.
Brilhaus, D., Bräutigam, A., Mettler-Altmann, T., Winter, K., & Weber, A. P. M. (2016). Reversible Burst of Transcriptional Changes during Induction of Crassulacean Acid Metabolism in Talinum triangulare. Plant Physiology, 170(1), 102-122. doi:10.1104/pp.15.01076
Brilhaus, D., Bräutigam, A., Mettler-Altmann, T., Winter, K., and Weber, A. P. M. (2016). Reversible Burst of Transcriptional Changes during Induction of Crassulacean Acid Metabolism in Talinum triangulare. Plant Physiology 170, 102-122.
Brilhaus, D., et al., 2016. Reversible Burst of Transcriptional Changes during Induction of Crassulacean Acid Metabolism in Talinum triangulare. Plant Physiology, 170(1), p 102-122.
D. Brilhaus, et al., “Reversible Burst of Transcriptional Changes during Induction of Crassulacean Acid Metabolism in Talinum triangulare”, Plant Physiology, vol. 170, 2016, pp. 102-122.
Brilhaus, D., Bräutigam, A., Mettler-Altmann, T., Winter, K., Weber, A.P.M.: Reversible Burst of Transcriptional Changes during Induction of Crassulacean Acid Metabolism in Talinum triangulare. Plant Physiology. 170, 102-122 (2016).
Brilhaus, Dominik, Bräutigam, Andrea, Mettler-Altmann, Tabea, Winter, Klaus, and Weber, Andreas P. M. “Reversible Burst of Transcriptional Changes during Induction of Crassulacean Acid Metabolism in Talinum triangulare”. Plant Physiology 170.1 (2016): 102-122.
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18 Zitationen in Europe PMC

Daten bereitgestellt von Europe PubMed Central.

Hierarchical clustering reveals unique features in the diel dynamics of metabolites in the CAM orchid Phalaenopsis.
Ceusters N, Luca S, Feil R, Claes JE, Lunn JE, Van den Ende W, Ceusters J., J Exp Bot 70(12), 2019
PMID: 30972416
Time of day and network reprogramming during drought induced CAM photosynthesis in Sedum album.
Wai CM, Weise SE, Ozersky P, Mockler TC, Michael TP, VanBuren R., PLoS Genet 15(6), 2019
PMID: 31199791
Altered Gene Regulatory Networks Are Associated With the Transition From C3 to Crassulacean Acid Metabolism in Erycina (Oncidiinae: Orchidaceae).
Heyduk K, Hwang M, Albert V, Silvera K, Lan T, Farr K, Chang TH, Chan MT, Winter K, Leebens-Mack J., Front Plant Sci 9(), 2018
PMID: 30745906
Shifts in gene expression profiles are associated with weak and strong Crassulacean acid metabolism.
Heyduk K, Ray JN, Ayyampalayam S, Leebens-Mack J., Am J Bot 105(3), 2018
PMID: 29746718
RNA-seq transcriptomic profiling of crassulacean acid metabolism pathway in Dendrobium catenatum.
Zou LH, Wan X, Deng H, Zheng BQ, Li BJ, Wang Y., Sci Data 5(), 2018
PMID: 30422119
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., Mol Plant 10(1), 2017
PMID: 27702693
Stomatal Biology of CAM Plants.
Males J, Griffiths H., Plant Physiol 174(2), 2017
PMID: 28242656
Secrets of succulence.
Males J., J Exp Bot 68(9), 2017
PMID: 28369497
On the Evolutionary Origin of CAM Photosynthesis.
Bräutigam A, Schlüter U, Eisenhut M, Gowik U., Plant Physiol 174(2), 2017
PMID: 28416703
Effect of Topical Iloprost and Nitroglycerin on Gastric Microcirculation and Barrier Function during Hemorrhagic Shock in Dogs.
Truse R, Hinterberg J, Schulz J, Herminghaus A, Weber A, Mettler-Altmann T, Bauer I, Picker O, Vollmer C., J Vasc Res 54(2), 2017
PMID: 28441653
Emerging model systems for functional genomics analysis of Crassulacean acid metabolism.
Hartwell J, Dever LV, Boxall SF., Curr Opin Plant Biol 31(), 2016
PMID: 27082281
Systems biology: A new CAM era.
Fernie AR., Nat Plants 2(), 2016
PMID: 27869788

84 References

Daten bereitgestellt von Europe PubMed Central.

Cis-regulatory code of stress-responsive transcription in Arabidopsis thaliana.
Zou C, Sun K, Mackaluso JD, Seddon AE, Jin R, Thomashow MF, Shiu SH., Proc. Natl. Acad. Sci. U.S.A. 108(36), 2011
PMID: 21849619
ABA-insensitive3, ABA-insensitive5, and DELLAs Interact to activate the expression of SOMNUS and other high-temperature-inducible genes in imbibed seeds in Arabidopsis.
Lim S, Park J, Lee N, Jeong J, Toh S, Watanabe A, Kim J, Kang H, Kim DH, Kawakami N, Choi G., Plant Cell 25(12), 2013
PMID: 24326588
A roadmap for research on crassulacean acid metabolism (CAM) to enhance sustainable food and bioenergy production in a hotter, drier world.
Yang X, Cushman JC, Borland AM, Edwards EJ, Wullschleger SD, Tuskan GA, Owen NA, Griffiths H, Smith JA, De Paoli HC, Weston DJ, Cottingham R, Hartwell J, Davis SC, Silvera K, Ming R, Schlauch K, Abraham P, Stewart JR, Guo HB, Albion R, Ha J, Lim SD, Wone BW, Yim WC, Garcia T, Mayer JA, Petereit J, Nair SS, Casey E, Hettich RL, Ceusters J, Ranjan P, Palla KJ, Yin H, Reyes-Garcia C, Andrade JL, Freschi L, Beltran JD, Dever LV, Boxall SF, Waller J, Davies J, Bupphada P, Kadu N, Winter K, Sage RF, Aguilar CN, Schmutz J, Jenkins J, Holtum JA., New Phytol. 207(3), 2015
PMID: 26153373
Abscisic acid inhibits type 2C protein phosphatases via the PYR/PYL family of START proteins.
Park SY, Fung P, Nishimura N, Jensen DR, Fujii H, Zhao Y, Lumba S, Santiago J, Rodrigues A, Chow TF, Alfred SE, Bonetta D, Finkelstein R, Provart NJ, Desveaux D, Rodriguez PL, McCourt P, Zhu JK, Schroeder JI, Volkman BF, Cutler SR., Science 324(5930), 2009
PMID: 19407142
MAPMAN: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes.
Thimm O, Blasing O, Gibon Y, Nagel A, Meyer S, Kruger P, Selbig J, Muller LA, Rhee SY, Stitt M., Plant J. 37(6), 2004
PMID: 14996223
BLAT--the BLAST-like alignment tool.
Kent WJ., Genome Res. 12(4), 2002
PMID: 11932250
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 influence of climate change on global crop productivity.
Lobell DB, Gourdji SM., Plant Physiol. 160(4), 2012
PMID: 23054565
Early light-induced proteins protect Arabidopsis from photooxidative stress.
Hutin C, Nussaume L, Moise N, Moya I, Kloppstech K, Havaux M., Proc. Natl. Acad. Sci. U.S.A. 100(8), 2003
PMID: 12676998
AtFtsH6 is involved in the degradation of the light-harvesting complex II during high-light acclimation and senescence.
Zelisko A, Garcia-Lorenzo M, Jackowski G, Jansson S, Funk C., Proc. Natl. Acad. Sci. U.S.A. 102(38), 2005
PMID: 16157880
Shared origins of a key enzyme during the evolution of C4 and CAM metabolism.
Christin PA, Arakaki M, Osborne CP, Brautigam A, Sage RF, Hibberd JM, Kelly S, Covshoff S, Wong GK, Hancock L, Edwards EJ., J. Exp. Bot. 65(13), 2014
PMID: 24638902
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
The CCCH-type zinc finger proteins AtSZF1 and AtSZF2 regulate salt stress responses in Arabidopsis.
Sun J, Jiang H, Xu Y, Li H, Wu X, Xie Q, Li C., Plant Cell Physiol. 48(8), 2007
PMID: 17609218
Predicting subcellular localization of proteins based on their N-terminal amino acid sequence.
Emanuelsson O, Nielsen H, Brunak S, von Heijne G., J. Mol. Biol. 300(4), 2000
PMID: 10891285
PlnTFDB: updated content and new features of the plant transcription factor database.
Perez-Rodriguez P, Riano-Pachon DM, Correa LG, Rensing SA, Kersten B, Mueller-Roeber B., Nucleic Acids Res. 38(Database issue), 2009
PMID: 19858103
Phosphoenolpyruvate carboxylase kinase is a novel protein kinase regulated at the level of expression.
Hartwell J, Gill A, Nimmo GA, Wilkins MB, Jenkins GI, Nimmo HG., Plant J. 20(3), 1999
PMID: 10571893
Salt and drought stress signal transduction in plants.
Zhu JK., Annu Rev Plant Biol 53(), 2002
PMID: 12221975
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
Type 2C protein phosphatases directly regulate abscisic acid-activated protein kinases in Arabidopsis.
Umezawa T, Sugiyama N, Mizoguchi M, Hayashi S, Myouga F, Yamaguchi-Shinozaki K, Ishihama Y, Hirayama T, Shinozaki K., Proc. Natl. Acad. Sci. U.S.A. 106(41), 2009
PMID: 19805022
Full-length transcriptome assembly from RNA-Seq data without a reference genome.
Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, Adiconis X, Fan L, Raychowdhury R, Zeng Q, Chen Z, Mauceli E, Hacohen N, Gnirke A, Rhind N, di Palma F, Birren BW, Nusbaum C, Lindblad-Toh K, Friedman N, Regev A., Nat. Biotechnol. 29(7), 2011
PMID: 21572440
Arabidopsis Cys2/His2-type zinc-finger proteins function as transcription repressors under drought, cold, and high-salinity stress conditions.
Sakamoto H, Maruyama K, Sakuma Y, Meshi T, Iwabuchi M, Shinozaki K, Yamaguchi-Shinozaki K., Plant Physiol. 136(1), 2004
PMID: 15333755
Galactinol and raffinose constitute a novel function to protect plants from oxidative damage.
Nishizawa A, Yabuta Y, Shigeoka S., Plant Physiol. 147(3), 2008
PMID: 18502973
BLAST+: architecture and applications.
Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J, Bealer K, Madden TL., BMC Bioinformatics 10(), 2009
PMID: 20003500
A central integrator of transcription networks in plant stress and energy signalling.
Baena-Gonzalez E, Rolland F, Thevelein JM, Sheen J., Nature 448(7156), 2007
PMID: 17671505
A cytosolic glucosyltransferase is required for conversion of starch to sucrose in Arabidopsis leaves at night.
Chia T, Thorneycroft D, Chapple A, Messerli G, Chen J, Zeeman SC, Smith SM, Smith AM., Plant J. 37(6), 2004
PMID: 14996213
Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega.
Sievers F, Wilm A, Dineen D, Gibson TJ, Karplus K, Li W, Lopez R, McWilliam H, Remmert M, Soding J, Thompson JD, Higgins DG., Mol. Syst. Biol. 7(), 2011
PMID: 21988835
Comprehensive transcriptome analysis of the highly complex Pisum sativum genome using next generation sequencing.
Franssen SU, Shrestha RP, Brautigam A, Bornberg-Bauer E, Weber AP., BMC Genomics 12(), 2011
PMID: 21569327
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
Plastidic metabolite transporters and their physiological functions in the inducible crassulacean acid metabolism plant Mesembryanthemum crystallinum.
Hausler RE, Baur B, Scharte J, Teichmann T, Eicks M, Fischer KL, Flugge UI, Schubert S, Weber A, Fischer K., Plant J. 24(3), 2000
PMID: 11069702
Circadian rhythms in the activity of a plant protein kinase.
Carter PJ, Nimmo HG, Fewson CA, Wilkins MB., EMBO J. 10(8), 1991
PMID: 2065654
The genome of the recently domesticated crop plant sugar beet (Beta vulgaris).
Dohm JC, Minoche AE, Holtgrawe D, Capella-Gutierrez S, Zakrzewski F, Tafer H, Rupp O, Sorensen TR, Stracke R, Reinhardt R, Goesmann A, Kraft T, Schulz B, Stadler PF, Schmidt T, Gabaldon T, Lehrach H, Weisshaar B, Himmelbauer H., Nature 505(7484), 2013
PMID: 24352233
A previously unknown maltose transporter essential for starch degradation in leaves.
Niittyla T, Messerli G, Trevisan M, Chen J, Smith AM, Zeeman SC., Science 303(5654), 2004
PMID: 14704427
SOMNUS, a CCCH-type zinc finger protein in Arabidopsis, negatively regulates light-dependent seed germination downstream of PIL5.
Kim DH, Yamaguchi S, Lim S, Oh E, Park J, Hanada A, Kamiya Y, Choi G., Plant Cell 20(5), 2008
PMID: 18487351
Improved scoring of functional groups from gene expression data by decorrelating GO graph structure.
Alexa A, Rahnenfuhrer J, Lengauer T., Bioinformatics 22(13), 2006
PMID: 16606683
Homeostasis of adenylate status during photosynthesis in a fluctuating environment.
Noctor G, Foyer CH., J. Exp. Bot. 51 Spec No(), 2000
PMID: 10938842
Adaptations to Environmental Stresses.
Bohnert HJ, Nelson DE, Jensen RG., Plant Cell 7(7), 1995
PMID: 12242400
RNA-Seq Assembly - Are We There Yet?
Schliesky S, Gowik U, Weber AP, Brautigam A., Front Plant Sci 3(), 2012
PMID: 23056003
The AtGenExpress hormone and chemical treatment data set: experimental design, data evaluation, model data analysis and data access.
Goda H, Sasaki E, Akiyama K, Maruyama-Nakashita A, Nakabayashi K, Li W, Ogawa M, Yamauchi Y, Preston J, Aoki K, Kiba T, Takatsuto S, Fujioka S, Asami T, Nakano T, Kato H, Mizuno T, Sakakibara H, Yamaguchi S, Nambara E, Kamiya Y, Takahashi H, Hirai MY, Sakurai T, Shinozaki K, Saito K, Yoshida S, Shimada Y., Plant J. 55(3), 2008
PMID: 18419781
Isolation and characterization of mutants of common ice plant deficient in crassulacean acid metabolism.
Cushman JC, Agarie S, Albion RL, Elliot SM, Taybi T, Borland AM., Plant Physiol. 147(1), 2008
PMID: 18326789
Closing gaps: linking elements that control stomatal movement.
Kollist H, Nuhkat M, Roelfsema MR., New Phytol. 203(1), 2014
PMID: 24800691
New insights on trehalose: a multifunctional molecule.
Elbein AD, Pan YT, Pastuszak I, Carroll D., Glycobiology 13(4), 2003
PMID: 12626396
Diurnal changes in the transcriptome encoding enzymes of starch metabolism provide evidence for both transcriptional and posttranscriptional regulation of starch metabolism in Arabidopsis leaves.
Smith SM, Fulton DC, Chia T, Thorneycroft D, Chapple A, Dunstan H, Hylton C, Zeeman SC, Smith AM., Plant Physiol. 136(1), 2004
PMID: 15347792
THE MOLECULAR BASIS OF DEHYDRATION TOLERANCE IN PLANTS.
Ingram J, Bartels D., Annu. Rev. Plant Physiol. Plant Mol. Biol. 47(), 1996
PMID: 15012294
New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0.
Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O., Syst. Biol. 59(3), 2010
PMID: 20525638
Identification, purification, and molecular cloning of a putative plastidic glucose translocator.
Weber A, Servaites JC, Geiger DR, Kofler H, Hille D, Groner F, Hebbeker U, Flugge UI., Plant Cell 12(5), 2000
PMID: 10810150
Abscisic acid: emergence of a core signaling network.
Cutler SR, Rodriguez PL, Finkelstein RR, Abrams SR., Annu Rev Plant Biol 61(), 2010
PMID: 20192755
Starch metabolism in Arabidopsis.
Streb S, Zeeman SC., Arabidopsis Book 10(), 2012
PMID: 23393426
Evolution of C4 phosphoenolpyruvate carboxylase.
Svensson P, Blasing OE, Westhoff P., Arch. Biochem. Biophys. 414(2), 2003
PMID: 12781769
Malate transport and vacuolar ion channels in CAM plants.
Cheffings CM, Pantoja O, Ashcroft FM, Smith JA., J. Exp. Bot. 48 Spec No(), 1997
PMID: 21245236
Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2.
Love MI, Huber W, Anders S., Genome Biol. 15(12), 2014
PMID: 25516281

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