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Chloroplasts are central players in sugar-induced leaf growth

Judith Van Dingenen, Liesbeth De Milde UGent, Mattias Vermeersch UGent, Katrien Maleux, Riet De Rycke UGent, Michiel De Bruyne UGent, Veronique Storme UGent, Nathalie Gonzalez Sanchez, Stijn Dhondt UGent and Dirk Inzé UGent (2016) PLANT PHYSIOLOGY. 171(1). p.590-605
abstract
Leaves are the plant's powerhouses, providing energy for all organs through sugar production during photosynthesis. However, sugars serve not only as a metabolic energy source for sink tissues but also as signaling molecules, affecting gene expression through conserved signaling pathways to regulate plant growth and development. Here, we describe an in vitro experimental assay, allowing one to alter the sucrose (Suc) availability during early Arabidopsis (Arabidopsis thaliana) leaf development, with the aim to identify the affected cellular and molecular processes. The transfer of seedlings to Suc-containing medium showed a profound effect on leaf growth by stimulating cell proliferation and postponing the transition to cell expansion. Furthermore, rapidly after transfer to Suc, mesophyll cells contained fewer and smaller plastids, which are irregular in shape and contain fewer starch granules compared with control mesophyll cells. Short-term transcriptional responses after transfer to Suc revealed the repression of well-known sugar-responsive genes and multiple genes encoded by the plastid, on the one hand, and up-regulation of a GLUCOSE-6-PHOSPHATE TRANSPORTER (GPT2), on the other hand. Mutant gpt2 seedlings showed no stimulation of cell proliferation and no repression of chloroplast-encoded transcripts when transferred to Suc, suggesting that GPT2 plays a critical role in the Suc-mediated effects on early leaf growth. Our findings, therefore, suggest that induction of GPT2 expression by Suc increases the import of glucose-6-phosphate into the plastids that would repress chloroplast-encoded transcripts, restricting chloroplast differentiation. Retrograde signaling from the plastids would then delay the transition to cell expansion and stimulate cell proliferation.
Please use this url to cite or link to this publication:
author
organization
year
type
journalArticle (original)
publication status
published
subject
keyword
RETROGRADE SIGNALS, DEVELOPING LEAVES, TRANSCRIPTION NETWORKS, TREHALOSE 6-PHOSPHATE, ARABIDOPSIS-THALIANA, PLANT-CELL CYCLE, GLUCOSE 6-PHOSPHATE/PHOSPHATE TRANSLOCATOR, NUCLEAR GENE-EXPRESSION, METABOLISM, HIGH LIGHT
journal title
PLANT PHYSIOLOGY
Plant Physiol.
volume
171
issue
1
pages
590 - 605
Web of Science type
Article
Web of Science id
000375431500045
JCR category
PLANT SCIENCES
JCR impact factor
6.456 (2016)
JCR rank
11/211 (2016)
JCR quartile
1 (2016)
ISSN
0032-0889
DOI
10.1104/pp.15.01669
project
Biotechnology for a sustainable economy (Bio-Economy)
language
English
UGent publication?
yes
classification
A1
copyright statement
I have retained and own the full copyright for this publication
id
7244197
handle
http://hdl.handle.net/1854/LU-7244197
date created
2016-06-06 13:06:18
date last changed
2017-07-03 10:30:31
@article{7244197,
  abstract     = {Leaves are the plant's powerhouses, providing energy for all organs through sugar production during photosynthesis. However, sugars serve not only as a metabolic energy source for sink tissues but also as signaling molecules, affecting gene expression through conserved signaling pathways to regulate plant growth and development. Here, we describe an in vitro experimental assay, allowing one to alter the sucrose (Suc) availability during early Arabidopsis (Arabidopsis thaliana) leaf development, with the aim to identify the affected cellular and molecular processes. The transfer of seedlings to Suc-containing medium showed a profound effect on leaf growth by stimulating cell proliferation and postponing the transition to cell expansion. Furthermore, rapidly after transfer to Suc, mesophyll cells contained fewer and smaller plastids, which are irregular in shape and contain fewer starch granules compared with control mesophyll cells. Short-term transcriptional responses after transfer to Suc revealed the repression of well-known sugar-responsive genes and multiple genes encoded by the plastid, on the one hand, and up-regulation of a GLUCOSE-6-PHOSPHATE TRANSPORTER (GPT2), on the other hand. Mutant gpt2 seedlings showed no stimulation of cell proliferation and no repression of chloroplast-encoded transcripts when transferred to Suc, suggesting that GPT2 plays a critical role in the Suc-mediated effects on early leaf growth. Our findings, therefore, suggest that induction of GPT2 expression by Suc increases the import of glucose-6-phosphate into the plastids that would repress chloroplast-encoded transcripts, restricting chloroplast differentiation. Retrograde signaling from the plastids would then delay the transition to cell expansion and stimulate cell proliferation.},
  author       = {Van Dingenen, Judith and De Milde, Liesbeth and Vermeersch, Mattias and Maleux, Katrien and De Rycke, Riet and De Bruyne, Michiel and Storme, Veronique and Gonzalez Sanchez, Nathalie and Dhondt, Stijn and Inz{\'e}, Dirk},
  issn         = {0032-0889},
  journal      = {PLANT PHYSIOLOGY},
  keyword      = {RETROGRADE SIGNALS,DEVELOPING LEAVES,TRANSCRIPTION NETWORKS,TREHALOSE 6-PHOSPHATE,ARABIDOPSIS-THALIANA,PLANT-CELL CYCLE,GLUCOSE 6-PHOSPHATE/PHOSPHATE TRANSLOCATOR,NUCLEAR GENE-EXPRESSION,METABOLISM,HIGH LIGHT},
  language     = {eng},
  number       = {1},
  pages        = {590--605},
  title        = {Chloroplasts are central players in sugar-induced leaf growth},
  url          = {http://dx.doi.org/10.1104/pp.15.01669},
  volume       = {171},
  year         = {2016},
}

Chicago
Van Dingenen, Judith, Liesbeth De Milde, Mattias Vermeersch, Katrien Maleux, Riet De Rycke, Michiel De Bruyne, Veronique Storme, Nathalie Gonzalez Sanchez, Stijn Dhondt, and Dirk Inzé. 2016. “Chloroplasts Are Central Players in Sugar-induced Leaf Growth.” Plant Physiology 171 (1): 590–605.
APA
Van Dingenen, Judith, De Milde, L., Vermeersch, M., Maleux, K., De Rycke, R., De Bruyne, M., Storme, V., et al. (2016). Chloroplasts are central players in sugar-induced leaf growth. PLANT PHYSIOLOGY, 171(1), 590–605.
Vancouver
1.
Van Dingenen J, De Milde L, Vermeersch M, Maleux K, De Rycke R, De Bruyne M, et al. Chloroplasts are central players in sugar-induced leaf growth. PLANT PHYSIOLOGY. 2016;171(1):590–605.
MLA
Van Dingenen, Judith, Liesbeth De Milde, Mattias Vermeersch, et al. “Chloroplasts Are Central Players in Sugar-induced Leaf Growth.” PLANT PHYSIOLOGY 171.1 (2016): 590–605. Print.