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Comparative transcriptome atlases reveal altered gene expression modules between two Cleomaceae C₃ and C₄ plant species

Canan Kulahoglu, Alisandra K Denton, Manuel Sommer, Janina Mass, Simon Schliesky, Thomas J Wrobel, Barbara Berckmans, Elsa Gongora-Castillo, C Robin Buell, Rüdiger Simon, et al. (2014) PLANT CELL. 26(8). p.3243-3260
abstract
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.
Please use this url to cite or link to this publication:
author
organization
alternative title
Comparative transcriptome atlases reveal altered gene expression modules between two Cleomaceae C-3 and C-4 plant species
year
type
journalArticle (original)
publication status
published
subject
keyword
CELL-PROLIFERATION, LEAF DEVELOPMENT, MESOPHYLL DEVELOPMENT, ORTHOPHOSPHATE DIKINASE, PHOSPHOENOLPYRUVATE/PHOSPHATE-TRANSLOCATOR, VEIN FORMATION, C4 PLANTS, GENOME-WIDE ANALYSIS, ARABIDOPSIS-THALIANA, ADAPTER PROTEIN
journal title
PLANT CELL
Plant Cell
volume
26
issue
8
pages
3243 - 3260
Web of Science type
Article
Web of Science id
000345918600004
JCR category
PLANT SCIENCES
JCR impact factor
9.338 (2014)
JCR rank
4/204 (2014)
JCR quartile
1 (2014)
ISSN
1040-4651
DOI
10.1105/tpc.114.123752
language
English
UGent publication?
yes
classification
A1
additional info
the first two authors contributed equally to this work
copyright statement
I have transferred the copyright for this publication to the publisher
id
5821736
handle
http://hdl.handle.net/1854/LU-5821736
date created
2015-01-27 10:37:19
date last changed
2016-12-19 15:39:47
@article{5821736,
  abstract     = {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.},
  author       = {Kulahoglu, Canan and Denton, Alisandra K and Sommer, Manuel and Mass, Janina and Schliesky, Simon and Wrobel, Thomas J and Berckmans, Barbara and Gongora-Castillo, Elsa and Buell, C Robin and Simon, R{\"u}diger and De Veylder, Lieven and Br{\"a}utigam, Andrea and Weber, Andreas PM},
  issn         = {1040-4651},
  journal      = {PLANT CELL},
  keyword      = {CELL-PROLIFERATION,LEAF DEVELOPMENT,MESOPHYLL DEVELOPMENT,ORTHOPHOSPHATE DIKINASE,PHOSPHOENOLPYRUVATE/PHOSPHATE-TRANSLOCATOR,VEIN FORMATION,C4 PLANTS,GENOME-WIDE ANALYSIS,ARABIDOPSIS-THALIANA,ADAPTER PROTEIN},
  language     = {eng},
  number       = {8},
  pages        = {3243--3260},
  title        = {Comparative transcriptome atlases reveal altered gene expression modules between two Cleomaceae C\unmatched{2083} and C\unmatched{2084} plant species},
  url          = {http://dx.doi.org/10.1105/tpc.114.123752},
  volume       = {26},
  year         = {2014},
}

Chicago
Kulahoglu, Canan, Alisandra K Denton, Manuel Sommer, Janina Mass, Simon Schliesky, Thomas J Wrobel, Barbara Berckmans, et al. 2014. “Comparative Transcriptome Atlases Reveal Altered Gene Expression Modules Between Two Cleomaceae C₃ and C₄ Plant Species.” Plant Cell 26 (8): 3243–3260.
APA
Kulahoglu, 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 C₃ and C₄ plant species. PLANT CELL, 26(8), 3243–3260.
Vancouver
1.
Kulahoglu C, Denton AK, Sommer M, Mass J, Schliesky S, Wrobel TJ, et al. Comparative transcriptome atlases reveal altered gene expression modules between two Cleomaceae C₃ and C₄ plant species. PLANT CELL. 2014;26(8):3243–60.
MLA
Kulahoglu, Canan, Alisandra K Denton, Manuel Sommer, et al. “Comparative Transcriptome Atlases Reveal Altered Gene Expression Modules Between Two Cleomaceae C₃ and C₄ Plant Species.” PLANT CELL 26.8 (2014): 3243–3260. Print.