Systems analysis of cis-regulatory motifs in C-4 photosynthesis genes using maize and rice leaf transcriptomic data during a process of de-etiolation

Xu J, Bräutigam A, Weber APM, Zhu X-G (2016)
Journal of Experimental Botany 67(17): 5105-5117.

Zeitschriftenaufsatz | Veröffentlicht | Englisch
OA 5.09 MB
Xu, Jiajia; Bräutigam, AndreaUniBi ; Weber, Andreas P. M.; Zhu, Xin-Guang
Abstract / Bemerkung
Identification of potential cis-regulatory motifs controlling the development of C-4 photosynthesis is a major focus of current research. In this study, we used time-series RNA-seq data collected from etiolated maize and rice leaf tissues sampled during a de-etiolation process to systematically characterize the expression patterns of C-4-related genes and to further identify potential cis elements in five different genomic regions (i.e. promoter, 5'UTR, 3'UTR, intron, and coding sequence) of C-4 orthologous genes. The results demonstrate that although most of the C-4 genes show similar expression patterns, a number of them, including chloroplast dicarboxylate transporter 1, aspartate aminotransferase, and triose phosphate transporter, show shifted expression patterns compared with their C-3 counterparts. A number of conserved short DNA motifs between maize C-4 genes and their rice orthologous genes were identified not only in the promoter, 5'UTR, 3'UTR, and coding sequences, but also in the introns of core C4 genes. We also identified cis-regulatory motifs that exist in maize C-4 genes and also in genes showing similar expression patterns as maize C-4 genes but that do not exist in rice C-3 orthologs, suggesting a possible recruitment of pre-existing cis-elements from genes unrelated to C-4 photosynthesis into C-4 photosynthesis genes during C-4 evolution.
C-4 photosynthesis; cell specificity; cis element; evolution; etiolation; systems biology
Journal of Experimental Botany
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Xu J, Bräutigam A, Weber APM, Zhu X-G. Systems analysis of cis-regulatory motifs in C-4 photosynthesis genes using maize and rice leaf transcriptomic data during a process of de-etiolation. Journal of Experimental Botany. 2016;67(17):5105-5117.
Xu, J., Bräutigam, A., Weber, A. P. M., & Zhu, X. - G. (2016). Systems analysis of cis-regulatory motifs in C-4 photosynthesis genes using maize and rice leaf transcriptomic data during a process of de-etiolation. Journal of Experimental Botany, 67(17), 5105-5117. doi:10.1093/jxb/erw275
Xu, J., Bräutigam, A., Weber, A. P. M., and Zhu, X. - G. (2016). Systems analysis of cis-regulatory motifs in C-4 photosynthesis genes using maize and rice leaf transcriptomic data during a process of de-etiolation. Journal of Experimental Botany 67, 5105-5117.
Xu, J., et al., 2016. Systems analysis of cis-regulatory motifs in C-4 photosynthesis genes using maize and rice leaf transcriptomic data during a process of de-etiolation. Journal of Experimental Botany, 67(17), p 5105-5117.
J. Xu, et al., “Systems analysis of cis-regulatory motifs in C-4 photosynthesis genes using maize and rice leaf transcriptomic data during a process of de-etiolation”, Journal of Experimental Botany, vol. 67, 2016, pp. 5105-5117.
Xu, J., Bräutigam, A., Weber, A.P.M., Zhu, X.-G.: Systems analysis of cis-regulatory motifs in C-4 photosynthesis genes using maize and rice leaf transcriptomic data during a process of de-etiolation. Journal of Experimental Botany. 67, 5105-5117 (2016).
Xu, Jiajia, Bräutigam, Andrea, Weber, Andreas P. M., and Zhu, Xin-Guang. “Systems analysis of cis-regulatory motifs in C-4 photosynthesis genes using maize and rice leaf transcriptomic data during a process of de-etiolation”. Journal of Experimental Botany 67.17 (2016): 5105-5117.
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2 Zitationen in Europe PMC

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PMID: 29915917
Genetic determinants controlling maize rubisco activase gene expression and a comparison with rice counterparts.
Zhang Y, Zhou Y, Sun Q, Deng D, Liu H, Chen S, Yin Z., BMC Plant Biol 19(1), 2019
PMID: 31412785

66 References

Daten bereitgestellt von Europe PubMed Central.

The role of proteins in C(3) plants prior to their recruitment into the C(4) pathway.
Aubry S, Brown NJ, Hibberd JM., J. Exp. Bot. 62(9), 2011
PMID: 21321052
MEME: discovering and analyzing DNA and protein sequence motifs.
Bailey TL, Williams N, Misleh C, Li WW., Nucleic Acids Res. 34(Web Server issue), 2006
PMID: 16845028
FootPrinter: A program designed for phylogenetic footprinting.
Blanchette M, Tompa M., Nucleic Acids Res. 31(13), 2003
PMID: 12824433
The activities of the photosynthetic carbon cycle enzymes of greening bean leaves
Bradbeer JW., 1969
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
Agronomic implications of C photosynthesis
Brown HR., 1999
Independent and parallel recruitment of preexisting mechanisms underlying C₄ photosynthesis.
Brown NJ, Newell CA, Stanley S, Chen JE, Perrin AJ, Kajala K, Hibberd JM., Science 331(6023), 2011
PMID: 21415351
Setaria viridis: a model for C4 photosynthesis.
Brutnell TP, Wang L, Swartwood K, Goldschmidt A, Jackson D, Zhu XG, Kellogg E, Van Eck J., Plant Cell 22(8), 2010
PMID: 20693355
OrthoMCL-DB: querying a comprehensive multi-species collection of ortholog groups.
Chen F, Mackey AJ, Stoeckert CJ Jr, Roos DS., Nucleic Acids Res. 34(Database issue), 2006
PMID: 16381887
Signalling in light-controlled development.
Deng XW, Quail PH., Semin. Cell Dev. Biol. 10(2), 1999
PMID: 10441064
Enhanced translation of a chloroplast-expressed RbcS gene restores small subunit levels and photosynthesis in nuclear RbcS antisense plants
Dhingra A, Portis AR, Daniell H., 2004
The most abundant protein in the world
Ellis RJ., 1979
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
cis-Regulatory elements for mesophyll-specific gene expression in the C4 plant Flaveria trinervia, the promoter of the C4 phosphoenolpyruvate carboxylase gene.
Gowik U, Burscheidt J, Akyildiz M, Schlue U, Koczor M, Streubel M, Westhoff P., Plant Cell 16(5), 2004
PMID: 15100398
You’re so vein: Bundle sheath physiology, phylogeny and evolution in C and C plants
Griffiths H, Weller G, Toy LFM, Dennis RJ., 2013
A Common histone modification code on C4 genes in maize and its conservation in Sorghum and Setaria italica.
Heimann L, Horst I, Perduns R, Dreesen B, Offermann S, Peterhansel C., Plant Physiol. 162(1), 2013
PMID: 23564230
The regulation of gene expression required for C4 photosynthesis.
Hibberd JM, Covshoff S., Annu Rev Plant Biol 61(), 2010
PMID: 20192753
Plant cis-acting regulatory DNA elements (PLACE) database: 1999.
Higo K, Ugawa Y, Iwamoto M, Korenaga T., Nucleic Acids Res. 27(1), 1999
PMID: 9847208
The Ensembl genome database project.
Hubbard T, Barker D, Birney E, Cameron G, Chen Y, Clark L, Cox T, Cuff J, Curwen V, Down T, Durbin R, Eyras E, Gilbert J, Hammond M, Huminiecki L, Kasprzyk A, Lehvaslaiho H, Lijnzaad P, Melsopp C, Mongin E, Pettett R, Pocock M, Potter S, Rust A, Schmidt E, Searle S, Slater G, Smith J, Spooner W, Stabenau A, Stalker J, Stupka E, Ureta-Vidal A, Vastrik I, Clamp M., Nucleic Acids Res. 30(1), 2002
PMID: 11752248
Finding transcription factor binding motifs for coregulated genes by combining sequence overrepresentation with cross-species conservation
Jia H, Li J., 2012
Multiple Arabidopsis genes primed for recruitment into C₄ photosynthesis.
Kajala K, Brown NJ, Williams BP, Borrill P, Taylor LE, Hibberd JM., Plant J. 69(1), 2011
PMID: 21883556
Mesophyll-specific, light and metabolic regulation of the C4 PPCZm1 promoter in transgenic maize.
Kausch AP, Owen TP Jr, Zachwieja SJ, Flynn AR, Sheen J., Plant Mol. Biol. 45(1), 2001
PMID: 11247600
MATCH: A tool for searching transcription factor binding sites in DNA sequences.
Kel AE, Gossling E, Reuter I, Cheremushkin E, Kel-Margoulis OV, Wingender E., Nucleic Acids Res. 31(13), 2003
PMID: 12824369
Cell position and light influence C4 versus C3 patterns of photosynthetic gene expression in maize.
Langdale JA, Zelitch I, Miller E, Nelson T., EMBO J. 7(12), 1988
PMID: 2850171
Fast gapped-read alignment with Bowtie 2.
Langmead B, Salzberg SL., Nat. Methods 9(4), 2012
PMID: 22388286
How introns influence and enhance eukaryotic gene expression.
Le Hir H, Nott A, Moore MJ., Trends Biochem. Sci. 28(4), 2003
PMID: 12713906
STAMP: a web tool for exploring DNA-binding motif similarities.
Mahony S, Benos PV., Nucleic Acids Res. 35(Web Server issue), 2007
PMID: 17478497
Expression of the C4 Me1 Gene from Flaveria bidentis Requires an Interaction between 5[prime] and 3[prime] Sequences.
Marshall JS, Stubbs JD, Chitty JA, Surin B, Taylor WC., Plant Cell 9(9), 1997
PMID: 12237394
TRANSFAC: transcriptional regulation, from patterns to profiles.
Matys V, Fricke E, Geffers R, Gossling E, Haubrock M, Hehl R, Hornischer K, Karas D, Kel AE, Kel-Margoulis OV, Kloos DU, Land S, Lewicki-Potapov B, Michael H, Munch R, Reuter I, Rotert S, Saxel H, Scheer M, Thiele S, Wingender E., Nucleic Acids Res. 31(1), 2003
PMID: 12520026
InParanoid 7: new algorithms and tools for eukaryotic orthology analysis.
Ostlund G, Schmitt T, Forslund K, Kostler T, Messina DN, Roopra S, Frings O, Sonnhammer EL., Nucleic Acids Res. 38(Database issue), 2009
PMID: 19892828
Phyloscan: locating transcription-regulating binding sites in mixed aligned and unaligned sequence data.
Palumbo MJ, Newberg LA., Nucleic Acids Res. 38(Web Server issue), 2010
PMID: 20435683
MoD Tools: regulatory motif discovery in nucleotide sequences from co-regulated or homologous genes.
Pavesi G, Mereghetti P, Zambelli F, Stefani M, Mauri G, Pesole G., Nucleic Acids Res. 34(Web Server issue), 2006
PMID: 16845071
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
Ribosome and transcript copy numbers, polysome occupancy and enzyme dynamics in Arabidopsis
Piques M, Schulze WX, Höhne M, Usadel B, Gibon Y, Rohwer J, Stitt M., 2009
SIGNAL SCAN 4.0: additional databases and sequence formats.
Prestridge DS., Comput. Appl. Biosci. 12(2), 1996
PMID: 8744779
Predicting transcription factor affinities to DNA from a biophysical model.
Roider HG, Kanhere A, Manke T, Vingron M., Bioinformatics 23(2), 2006
PMID: 17098775
Finding DNA regulatory motifs within unaligned noncoding sequences clustered by whole-genome mRNA quantitation.
Roth FP, Hughes JD, Estep PW, Church GM., Nat. Biotechnol. 16(10), 1998
PMID: 9788350
The C(4) plant lineages of planet Earth.
Sage RF, Christin PA, Edwards EJ., J. Exp. Bot. 62(9), 2011
PMID: 21414957
Exploiting the engine of C(4) photosynthesis.
Sage RF, Zhu XG., J. Exp. Bot. 62(9), 2011
PMID: 21652533
Sheen J., Annu. Rev. Plant Physiol. Plant Mol. Biol. 50(), 1999
PMID: 15012208
Label-free quantitative proteomics analysis of etiolated maize seedling leaves during greening.
Shen Z, Li P, Ni RJ, Ritchie M, Yang CP, Liu GF, Ma W, Liu GJ, Ma L, Li SJ, Wei ZG, Wang HX, Wang BC., Mol. Cell Proteomics 8(11), 2009
PMID: 19666873
PhyME: a probabilistic algorithm for finding motifs in sets of orthologous sequences.
Sinha S, Blanchette M, Tompa M., BMC Bioinformatics 5(), 2004
PMID: 15511292
Phosphoenolpyruvate carboxykinase plays a role in interactions of carbon and nitrogen metabolism during grape seed development
Walker RP, Chen ZH, Tecsi LI, Famiani F, Lea PJ, Leegood RC., Planta 210(1), 1999
PMID: 10592027
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
Molecular evolution of genes recruited into C₄ photosynthesis.
Williams BP, Aubry S, Hibberd JM., Trends Plant Sci. 17(4), 2012
PMID: 22326564
An Untranslated cis-Element Regulates the Accumulation of Multiple C4 Enzymes in Gynandropsis gynandra Mesophyll Cells.
Williams BP, Burgess SJ, Reyna-Llorens I, Knerova J, Aubry S, Stanley S, Hibberd JM., Plant Cell 28(2), 2016
PMID: 26772995
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
PMID: 18374559


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