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Regulation of chloroplast gene expression in higher plants

Furo Tullberg, Anna LU (1998)
Abstract
Chloroplast gene expression is regulated by developmental and environmental signals. It has been proposed that there is a direct coupling between electron transport in biological membranes and gene expression (J. F. Allen, 1992, Biochim. Biophys. Acta 1098, 275-335). The hypothesis predicts the existence of a sensor in the thylakoid membrane capable of transmitting redox signals to the chloroplast genetic machinery. A contribution towards identifying the sensor is made by the discovery of a protein tyrosine kinase (PTK) activity in the thylakoid membrane which phosphorylates light harvesting complex II (LHC II) proteins.



To test whether variations in electron flow affected transcription of chloroplast genes, we produced... (More)
Chloroplast gene expression is regulated by developmental and environmental signals. It has been proposed that there is a direct coupling between electron transport in biological membranes and gene expression (J. F. Allen, 1992, Biochim. Biophys. Acta 1098, 275-335). The hypothesis predicts the existence of a sensor in the thylakoid membrane capable of transmitting redox signals to the chloroplast genetic machinery. A contribution towards identifying the sensor is made by the discovery of a protein tyrosine kinase (PTK) activity in the thylakoid membrane which phosphorylates light harvesting complex II (LHC II) proteins.



To test whether variations in electron flow affected transcription of chloroplast genes, we produced imbalances in electron flow in mustard (Sinapis alba, L.) and pea (Pisum sativum, L.) seedlings by illumination with different light qualities. The same effect was achieved in vitro by using specific inhibitors of electron transport. The effect of the modulations in electron flow on the transcription rates of chloroplast-encoded genes was analysed in chloroplast run-on transcription assays and revealed that the transcription rate of the psaB gene, coding for one of the reaction centre proteins of PS I, is under direct control of the redox-state of the plastoquinone (PQ) pool: reduction of the pool results in increased transcription rates of the psaB gene, while oxidation of the pool gives the opposite effect.



In vitro studies with isolated pea chloroplasts point to redox regulation of gene expression at the post-transcriptional level for the petB gene, coding for cytochrome b6 of the cytochrome b6f complex. In this case, we used chemical redox agents to assess stability of petB-containing messages. Under reducing conditions, petB mRNA does not exhibit altered stability compared to control chloroplasts; oxidising conditions cause almost complete degradation of petB mRNA molecules.



It is proposed that the first event in chloroplast redox signalling is the phosphorylation of a membrane-bound PTK in response to the redox state of the PQ pool, which could be the starting point of a signalling cascade affecting transcription and transcript stability of chloroplast-encoded genes such as psaB and petB, respectively. (Less)
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author
supervisor
opponent
  • Prof. Mayfield, Stephen P., Department of Cell Biology and Skaggs Institute for Chemical Biology, The Scripps Research Institute, La Jolla, California, USA
organization
publishing date
type
Thesis
publication status
published
subject
keywords
protein tyrosine kinase, plastoquinone pool, redox, Pisum sativum, Sinapis alba, petB, psaB, chloroplast, gene expression, Physiological biophysics, Växtfysiologi, light harvesting complex II
pages
114 pages
publisher
Department of Plant Cell Biology, Lund University
defense location
Lecture Hall of the Section of Plant Biology, Sölvegatan 35, Lund
defense date
1998-12-04 13:15:00
external identifiers
  • other:ISRN: LUNBDS/NBFB-98/1035/1-114-se
ISBN
91-628-3153-4
language
English
LU publication?
yes
additional info
Article: A protein tyrosine kinase of chloroplast thylakoid membranes phosphorylates light harvesting complex II proteins.Tullberg, A., Håkansson, G. and Race, H.L. (1998)Biochem. Biophys. Res. Commun. 250: 617-622. Article: The redox state of the chloroplast plastoquinone pool controls photosystem stoichiometry by direct transcriptional regulation of psaAB gene expression in mustard (Sinapis alba, L.).Pfannschmidt, T., Nilsson, A., Tullberg, A., Link, G. and Allen, J.F. (1998)submitted. Article: Photosynthetic electron flow regulates the transcription of the psaB gene in pea (Pisum sativum, L.) chloroplasts through the redox state of the plastoquinone pool.Tullberg, A., Alexciev, K., Pfannschmidt, T. and Allen, J.F. (1998)manuscript. Article: Regulation of petB mRNA stability in pea chloroplasts by redox poise.Alexciev, K. and Tullberg, A. (1997)Physiol. Plant. 99, 477-485.
id
524b4b58-b247-4806-961c-3d185537af63 (old id 39140)
date added to LUP
2016-04-04 11:55:58
date last changed
2018-11-21 21:08:03
@phdthesis{524b4b58-b247-4806-961c-3d185537af63,
  abstract     = {{Chloroplast gene expression is regulated by developmental and environmental signals. It has been proposed that there is a direct coupling between electron transport in biological membranes and gene expression (J. F. Allen, 1992, Biochim. Biophys. Acta 1098, 275-335). The hypothesis predicts the existence of a sensor in the thylakoid membrane capable of transmitting redox signals to the chloroplast genetic machinery. A contribution towards identifying the sensor is made by the discovery of a protein tyrosine kinase (PTK) activity in the thylakoid membrane which phosphorylates light harvesting complex II (LHC II) proteins.<br/><br>
<br/><br>
To test whether variations in electron flow affected transcription of chloroplast genes, we produced imbalances in electron flow in mustard (Sinapis alba, L.) and pea (Pisum sativum, L.) seedlings by illumination with different light qualities. The same effect was achieved in vitro by using specific inhibitors of electron transport. The effect of the modulations in electron flow on the transcription rates of chloroplast-encoded genes was analysed in chloroplast run-on transcription assays and revealed that the transcription rate of the psaB gene, coding for one of the reaction centre proteins of PS I, is under direct control of the redox-state of the plastoquinone (PQ) pool: reduction of the pool results in increased transcription rates of the psaB gene, while oxidation of the pool gives the opposite effect.<br/><br>
<br/><br>
In vitro studies with isolated pea chloroplasts point to redox regulation of gene expression at the post-transcriptional level for the petB gene, coding for cytochrome b6 of the cytochrome b6f complex. In this case, we used chemical redox agents to assess stability of petB-containing messages. Under reducing conditions, petB mRNA does not exhibit altered stability compared to control chloroplasts; oxidising conditions cause almost complete degradation of petB mRNA molecules.<br/><br>
<br/><br>
It is proposed that the first event in chloroplast redox signalling is the phosphorylation of a membrane-bound PTK in response to the redox state of the PQ pool, which could be the starting point of a signalling cascade affecting transcription and transcript stability of chloroplast-encoded genes such as psaB and petB, respectively.}},
  author       = {{Furo Tullberg, Anna}},
  isbn         = {{91-628-3153-4}},
  keywords     = {{protein tyrosine kinase; plastoquinone pool; redox; Pisum sativum; Sinapis alba; petB; psaB; chloroplast; gene expression; Physiological biophysics; Växtfysiologi; light harvesting complex II}},
  language     = {{eng}},
  publisher    = {{Department of Plant Cell Biology, Lund University}},
  school       = {{Lund University}},
  title        = {{Regulation of chloroplast gene expression in higher plants}},
  year         = {{1998}},
}