Comparative Transcriptome Atlases Reveal Altered Gene Expression Modules between Two Cleomaceae C-3 and C-4 Plant Species
Külahoglu C, Denton AK, Sommer M, Mass J, Schliesky S, Wrobel TJ, Berckmans B, Gongora-Castillo E, Buell CR, Simon R, De Veylder L, et al. (2014)
Plant Cell 26(8): 3243-3260.
Zeitschriftenaufsatz
| Veröffentlicht | Englisch
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Autor*in
Külahoglu, Canan;
Denton, Alisandra K.;
Sommer, Manuel;
Mass, Janina;
Schliesky, Simon;
Wrobel, Thomas J.;
Berckmans, Barbara;
Gongora-Castillo, Elsa;
Buell, C. Robin;
Simon, Ruediger;
De Veylder, Lieven;
Bräutigam, AndreaUniBi
Alle
Alle
Einrichtung
Abstract / Bemerkung
C-4 photosynthesis outperforms the ancestral C-3 state in a wide range of natural and agro-ecosystems by affording higher water-use and nitrogen-use efficiencies. It therefore represents a prime target for engineering novel, high-yielding crops by introducing the trait into C-3 backgrounds. However, the genetic architecture of C-4 photosynthesis remains largely unknown. To define the divergence in gene expression modules between C-3 and C-4 photosynthesis during leaf ontogeny, we generated comprehensive transcriptome atlases of two Cleomaceae species, Gynandropsis gynandra (C-4) and Tarenaya hassleriana (C-3), by RNA sequencing. Overall, the gene expression profiles appear remarkably similar between the C-3 and C-4 species. We found that known C-4 genes were recruited to photosynthesis from different expression domains in C-3, including typical housekeeping gene expression patterns in various tissues as well as individual heterotrophic tissues. Furthermore, we identified a structure-related module recruited from the C-3 root. Comparison of gene expression patterns with anatomy during leaf ontogeny provided insight into genetic features of Kranz anatomy. Altered expression of developmental factors and cell cycle genes is associated with a higher degree of endoreduplication in enlarged C-4 bundle sheath cells. A delay in mesophyll differentiation apparent both in the leaf anatomy and the transcriptome allows for extended vein formation in the C-4 leaf.
Erscheinungsjahr
2014
Zeitschriftentitel
Plant Cell
Band
26
Ausgabe
8
Seite(n)
3243-3260
ISSN
1040-4651
eISSN
1532-298X
Page URI
https://pub.uni-bielefeld.de/record/2915134
Zitieren
Külahoglu C, Denton AK, Sommer M, et al. Comparative Transcriptome Atlases Reveal Altered Gene Expression Modules between Two Cleomaceae C-3 and C-4 Plant Species. Plant Cell. 2014;26(8):3243-3260.
Külahoglu, C., Denton, A. K., Sommer, M., Mass, J., Schliesky, S., Wrobel, T. J., Berckmans, B., et al. (2014). Comparative Transcriptome Atlases Reveal Altered Gene Expression Modules between Two Cleomaceae C-3 and C-4 Plant Species. Plant Cell, 26(8), 3243-3260. doi:10.1105/tpc.114.123752
Külahoglu, Canan, Denton, Alisandra K., Sommer, Manuel, Mass, Janina, Schliesky, Simon, Wrobel, Thomas J., Berckmans, Barbara, et al. 2014. “Comparative Transcriptome Atlases Reveal Altered Gene Expression Modules between Two Cleomaceae C-3 and C-4 Plant Species”. Plant Cell 26 (8): 3243-3260.
Külahoglu, C., Denton, A. K., Sommer, M., Mass, J., Schliesky, S., Wrobel, T. J., Berckmans, B., Gongora-Castillo, E., Buell, C. R., Simon, R., et al. (2014). Comparative Transcriptome Atlases Reveal Altered Gene Expression Modules between Two Cleomaceae C-3 and C-4 Plant Species. Plant Cell 26, 3243-3260.
Külahoglu, C., et al., 2014. Comparative Transcriptome Atlases Reveal Altered Gene Expression Modules between Two Cleomaceae C-3 and C-4 Plant Species. Plant Cell, 26(8), p 3243-3260.
C. Külahoglu, et al., “Comparative Transcriptome Atlases Reveal Altered Gene Expression Modules between Two Cleomaceae C-3 and C-4 Plant Species”, Plant Cell, vol. 26, 2014, pp. 3243-3260.
Külahoglu, C., Denton, A.K., Sommer, M., Mass, J., Schliesky, S., Wrobel, T.J., Berckmans, B., Gongora-Castillo, E., Buell, C.R., Simon, R., De Veylder, L., Bräutigam, A., Weber, A.P.M.: Comparative Transcriptome Atlases Reveal Altered Gene Expression Modules between Two Cleomaceae C-3 and C-4 Plant Species. Plant Cell. 26, 3243-3260 (2014).
Külahoglu, Canan, Denton, Alisandra K., Sommer, Manuel, Mass, Janina, Schliesky, Simon, Wrobel, Thomas J., Berckmans, Barbara, Gongora-Castillo, Elsa, Buell, C. Robin, Simon, Ruediger, De Veylder, Lieven, Bräutigam, Andrea, and Weber, Andreas P. M. “Comparative Transcriptome Atlases Reveal Altered Gene Expression Modules between Two Cleomaceae C-3 and C-4 Plant Species”. Plant Cell 26.8 (2014): 3243-3260.
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2019-09-06T09:18:54Z
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Shifts in leaf vein density through accelerated vein formation in C4 Flaveria (Asteraceae).
McKown AD, Dengler NG., Ann. Bot. 104(6), 2009
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Endoreplication: polyploidy with purpose.
Lee HO, Davidson JM, Duronio RJ., Genes Dev. 23(21), 2009
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Robinson MD, McCarthy DJ, Smyth GK., Bioinformatics 26(1), 2009
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Robinson MD, McCarthy DJ, Smyth GK., Bioinformatics 26(1), 2009
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Ilegems M, Douet V, Meylan-Bettex M, Uyttewaal M, Brand L, Bowman JL, Stieger PA., Development 137(6), 2010
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The origins of C4 grasslands: integrating evolutionary and ecosystem science.
Edwards EJ, Osborne CP, Stromberg CA, Smith SA; C4 Grasses Consortium, Bond WJ, Christin PA, Cousins AB, Duvall MR, Fox DL, Freckleton RP, Ghannoum O, Hartwell J, Huang Y, Janis CM, Keeley JE, Kellogg EA, Knapp AK, Leakey AD, Nelson DM, Saarela JM, Sage RF, Sala OE, Salamin N, Still CJ, Tipple B., Science 328(5978), 2010
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Edwards EJ, Osborne CP, Stromberg CA, Smith SA; C4 Grasses Consortium, Bond WJ, Christin PA, Cousins AB, Duvall MR, Fox DL, Freckleton RP, Ghannoum O, Hartwell J, Huang Y, Janis CM, Keeley JE, Kellogg EA, Knapp AK, Leakey AD, Nelson DM, Saarela JM, Sage RF, Sala OE, Salamin N, Still CJ, Tipple B., Science 328(5978), 2010
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SIAMESE cooperates with the CDH1-like protein CCS52A1 to establish endoreplication in Arabidopsis thaliana trichomes.
Kasili R, Walker JD, Simmons LA, Zhou J, De Veylder L, Larkin JC., Genetics 185(1), 2010
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VND-INTERACTING2, a NAC domain transcription factor, negatively regulates xylem vessel formation in Arabidopsis.
Yamaguchi M, Ohtani M, Mitsuda N, Kubo M, Ohme-Takagi M, Fukuda H, Demura T., Plant Cell 22(4), 2010
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Putative Arabidopsis transcriptional adaptor protein (PROPORZ1) is required to modulate histone acetylation in response to auxin.
Anzola JM, Sieberer T, Ortbauer M, Butt H, Korbei B, Weinhofer I, Mullner AE, Luschnig C., Proc. Natl. Acad. Sci. U.S.A. 107(22), 2010
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Tronconi MA, Gerrard Wheeler MC, Maurino VG, Drincovich MF, Andreo CS., Biochem. J. 430(2), 2010
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Evolution of C4 photosynthesis--looking for the master switch.
Westhoff P, Gowik U., Plant Physiol. 154(2), 2010
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A role for AUXIN RESISTANT3 in the coordination of leaf growth.
Perez-Perez JM, Candela H, Robles P, Lopez-Torrejon G, del Pozo JC, Micol JL., Plant Cell Physiol. 51(10), 2010
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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
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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
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Exit from proliferation during leaf development in Arabidopsis thaliana: a not-so-gradual process.
Andriankaja M, Dhondt S, De Bodt S, Vanhaeren H, Coppens F, De Milde L, Muhlenbock P, Skirycz A, Gonzalez N, Beemster GT, Inze D., Dev. Cell 22(1), 2012
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Endoreduplication and development: rule without dividing?
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The phosphoenolpyruvate/phosphate translocator is required for phenolic metabolism, palisade cell development, and plastid-dependent nuclear gene expression.
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The future of C4 research--maize, Flaveria or Cleome?
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Genome-wide analysis of gene expression profiles associated with cell cycle transitions in growing organs of Arabidopsis.
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The Tarenaya hassleriana genome provides insight into reproductive trait and genome evolution of crucifers.
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Plastid signals and the bundle sheath: mesophyll development in reticulate mutants.
Lundquist PK, Rosar C, Brautigam A, Weber AP., Mol Plant 7(1), 2013
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Endoreduplication is not involved in bundle-sheath formation in the C4 species Cleome gynandra.
Aubry S, Knerova J, Hibberd JM., J. Exp. Bot. 65(13), 2013
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Aubry S, Knerova J, Hibberd JM., J. Exp. Bot. 65(13), 2013
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Towards an integrative model of C4 photosynthetic subtypes: insights from comparative transcriptome analysis of NAD-ME, NADP-ME, and PEP-CK C4 species.
Brautigam A, Schliesky S, Kulahoglu C, Osborne CP, Weber AP., J. Exp. Bot. 65(13), 2014
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Brautigam A, Schliesky S, Kulahoglu C, Osborne CP, Weber AP., J. Exp. Bot. 65(13), 2014
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Genome-wide analysis of core cell cycle genes in Arabidopsis.
Vandepoele K, Raes J, De Veylder L, Rouze P, Rombauts S, Inze D., Plant Cell 14(4), 2002
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Vandepoele K, Raes J, De Veylder L, Rouze P, Rombauts S, Inze D., Plant Cell 14(4), 2002
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Analysis of the plastidic phosphate translocator gene family in Arabidopsis and identification of new phosphate translocator-homologous transporters, classified by their putative substrate-binding site.
Knappe S, Flugge UI, Fischer K., Plant Physiol. 131(3), 2003
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Knappe S, Flugge UI, Fischer K., Plant Physiol. 131(3), 2003
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PROPORZ1, a putative Arabidopsis transcriptional adaptor protein, mediates auxin and cytokinin signals in the control of cell proliferation.
Sieberer T, Hauser MT, Seifert GJ, Luschnig C., Curr. Biol. 13(10), 2003
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Sieberer T, Hauser MT, Seifert GJ, Luschnig C., Curr. Biol. 13(10), 2003
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"Big it up": endoreduplication and cell-size control in plants.
Sugimoto-Shirasu K, Roberts K., Curr. Opin. Plant Biol. 6(6), 2003
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Sugimoto-Shirasu K, Roberts K., Curr. Opin. Plant Biol. 6(6), 2003
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A comprehensive analysis of the NADP-malic enzyme gene family of Arabidopsis.
Wheeler MC, Tronconi MA, Drincovich MF, Andreo CS, Flugge UI, Maurino VG., Plant Physiol. 139(1), 2005
PMID: 16113210
Wheeler MC, Tronconi MA, Drincovich MF, Andreo CS, Flugge UI, Maurino VG., Plant Physiol. 139(1), 2005
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Is C4 photosynthesis less phenotypically plastic than C3 photosynthesis?
Sage RF, McKown AD., J. Exp. Bot. 57(2), 2005
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Sage RF, McKown AD., J. Exp. Bot. 57(2), 2005
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Control of leaf vascular patterning by polar auxin transport.
Scarpella E, Marcos D, Friml J, Berleth T., Genes Dev. 20(8), 2006
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Scarpella E, Marcos D, Friml J, Berleth T., Genes Dev. 20(8), 2006
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Pvclust: an R package for assessing the uncertainty in hierarchical clustering.
Suzuki R, Shimodaira H., Bioinformatics 22(12), 2006
PMID: 16595560
Suzuki R, Shimodaira H., Bioinformatics 22(12), 2006
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Cleome, a genus closely related to Arabidopsis, contains species spanning a developmental progression from C(3) to C(4) photosynthesis.
Marshall DM, Muhaidat R, Brown NJ, Liu Z, Stanley S, Griffiths H, Sage RF, Hibberd JM., Plant J. 51(5), 2007
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Marshall DM, Muhaidat R, Brown NJ, Liu Z, Stanley S, Griffiths H, Sage RF, Hibberd JM., Plant J. 51(5), 2007
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Modification of cell proliferation patterns alters leaf vein architecture in Arabidopsis thaliana.
Kang J, Mizukami Y, Wang H, Fowke L, Dengler NG., Planta 226(5), 2007
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Kang J, Mizukami Y, Wang H, Fowke L, Dengler NG., Planta 226(5), 2007
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Specialization of CDC27 function in the Arabidopsis thaliana anaphase-promoting complex (APC/C).
Perez-Perez JM, Serralbo O, Vanstraelen M, Gonzalez C, Criqui MC, Genschik P, Kondorosi E, Scheres B., Plant J. 53(1), 2007
PMID: 17944809
Perez-Perez JM, Serralbo O, Vanstraelen M, Gonzalez C, Criqui MC, Genschik P, Kondorosi E, Scheres B., Plant J. 53(1), 2007
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The transcription factor MtSERF1 of the ERF subfamily identified by transcriptional profiling is required for somatic embryogenesis induced by auxin plus cytokinin in Medicago truncatula.
Mantiri FR, Kurdyukov S, Lohar DP, Sharopova N, Saeed NA, Wang XD, Vandenbosch KA, Rose RJ., Plant Physiol. 146(4), 2008
PMID: 18235037
Mantiri FR, Kurdyukov S, Lohar DP, Sharopova N, Saeed NA, Wang XD, Vandenbosch KA, Rose RJ., Plant Physiol. 146(4), 2008
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What is the maximum efficiency with which photosynthesis can convert solar energy into biomass?
Zhu XG, Long SP, Ort DR., Curr. Opin. Biotechnol. 19(2), 2008
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Zhu XG, Long SP, Ort DR., Curr. Opin. Biotechnol. 19(2), 2008
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Transcriptional regulation of vascular cell fates.
Ohashi-Ito K, Fukuda H., Curr. Opin. Plant Biol. 13(6), 2010
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Ohashi-Ito K, Fukuda H., Curr. Opin. Plant Biol. 13(6), 2010
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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
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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
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The Anaphase Promoting Complex activator CCS52A, a key factor for fruit growth and endoreduplication in Tomato.
Mathieu-Rivet E, Gevaudant F, Cheniclet C, Hernould M, Chevalier C., Plant Signal Behav 5(8), 2010
PMID: 20671429
Mathieu-Rivet E, Gevaudant F, Cheniclet C, Hernould M, Chevalier C., Plant Signal Behav 5(8), 2010
PMID: 20671429
Elucidating the functional role of endoreduplication in tomato fruit development.
Chevalier C, Nafati M, Mathieu-Rivet E, Bourdon M, Frangne N, Cheniclet C, Renaudin JP, Gevaudant F, Hernould M., Ann. Bot. 107(7), 2011
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Chevalier C, Nafati M, Mathieu-Rivet E, Bourdon M, Frangne N, Cheniclet C, Renaudin JP, Gevaudant F, Hernould M., Ann. Bot. 107(7), 2011
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The C(4) plant lineages of planet Earth.
Sage RF, Christin PA, Edwards EJ., J. Exp. Bot. 62(9), 2011
PMID: 21414957
Sage RF, Christin PA, Edwards EJ., J. Exp. Bot. 62(9), 2011
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Functional evolution of C(4) pyruvate, orthophosphate dikinase.
Chastain CJ, Failing CJ, Manandhar L, Zimmerman MA, Lakner MM, Nguyen TH., J. Exp. Bot. 62(9), 2011
PMID: 21414960
Chastain CJ, Failing CJ, Manandhar L, Zimmerman MA, Lakner MM, Nguyen TH., J. Exp. Bot. 62(9), 2011
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Exploiting the engine of C(4) photosynthesis.
Sage RF, Zhu XG., J. Exp. Bot. 62(9), 2011
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Sage RF, Zhu XG., J. Exp. Bot. 62(9), 2011
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Elevation of free proline and proline-rich protein levels by simultaneous manipulations of proline biosynthesis and degradation in plants.
Stein H, Honig A, Miller G, Erster O, Eilenberg H, Csonka LN, Szabados L, Koncz C, Zilberstein A., Plant Sci. 181(2), 2011
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Stein H, Honig A, Miller G, Erster O, Eilenberg H, Csonka LN, Szabados L, Koncz C, Zilberstein A., Plant Sci. 181(2), 2011
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Computational analysis of storage synthesis in developing Brassica napus L. (oilseed rape) embryos: flux variability analysis in relation to ¹³C metabolic flux analysis.
Hay J, Schwender J., Plant J. 67(3), 2011
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Hay J, Schwender J., Plant J. 67(3), 2011
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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
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
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Light-regulated and cell-specific methylation of the maize PEPC promoter.
Tolley BJ, Woodfield H, Wanchana S, Bruskiewich R, Hibberd JM., J. Exp. Bot. 63(3), 2011
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Tolley BJ, Woodfield H, Wanchana S, Bruskiewich R, Hibberd JM., J. Exp. Bot. 63(3), 2011
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Scarecrow plays a role in establishing Kranz anatomy in maize leaves.
Slewinski TL, Anderson AA, Zhang C, Turgeon R., Plant Cell Physiol. 53(12), 2012
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Slewinski TL, Anderson AA, Zhang C, Turgeon R., Plant Cell Physiol. 53(12), 2012
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GTL1 keeps cell growth and nuclear ploidy under control.
Caro E, Desvoyes B, Gutierrez C., EMBO J. 31(24), 2012
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Caro E, Desvoyes B, Gutierrez C., EMBO J. 31(24), 2012
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Transcriptional repression of the APC/C activator CCS52A1 promotes active termination of cell growth.
Breuer C, Morohashi K, Kawamura A, Takahashi N, Ishida T, Umeda M, Grotewold E, Sugimoto K., EMBO J. 31(24), 2012
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Breuer C, Morohashi K, Kawamura A, Takahashi N, Ishida T, Umeda M, Grotewold E, Sugimoto K., EMBO J. 31(24), 2012
PMID: 23143274
Brassinosteroid production and signaling differentially control cell division and expansion in the leaf.
Zhiponova MK, Vanhoutte I, Boudolf V, Betti C, Dhondt S, Coppens F, Mylle E, Maes S, Gonzalez-Garcia MP, Cano-Delgado AI, Inze D, Beemster GT, De Veylder L, Russinova E., New Phytol. 197(2), 2012
PMID: 23253334
Zhiponova MK, Vanhoutte I, Boudolf V, Betti C, Dhondt S, Coppens F, Mylle E, Maes S, Gonzalez-Garcia MP, Cano-Delgado AI, Inze D, Beemster GT, De Veylder L, Russinova E., New Phytol. 197(2), 2012
PMID: 23253334
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