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Coordination of two different genomes in response to light and stress
Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC). Umeå University, Faculty of Science and Technology, Department of Plant Physiology. (Åsa Strand)ORCID iD: 0000-0003-2061-1477
2016 (English)Doctoral thesis, comprehensive summary (Other academic)Alternative title
Hur två olika genom samarbetar under ljus och stress respons (Swedish)
Abstract [en]

About 1.5 billion years ago, a photosynthetic bacteria was engulfed by a eukaryotic cell which initiated a symbiotic relationship and the evolution of the chloroplast as we know it today. The chloroplast has retained its own genome encoding for a number of proteins required for the function of the chloroplast. However, during the evolution most genes were transferred to the nucleus and the chloroplast is thus dependent on the nucleus to provide the majority of proteins necessary for its function. The distribution of genes encoding plastid proteins between two different cellular compartments requires a tight communication in order to coordinate gene expression during different growth conditions. The focus of my PhD studies has been to elucidate signalling pathways between the chloroplast and nucleus that enables the coordination of these two genomes in response to light and stress. The results in this thesis demonstrate that chloroplast retrograde signals triggered by changes in tetrapyrrole levels are important both in response to day-night cycles and during the response to stress. We identified a cytosolic regulatory complex and a novel mechanism that could explain how the tetrapyrrole-mediated signal can be transduced from the plastid to the nucleus and regulate nuclear gene expression in response to changes in the environment. My work further demonstrates that the tetrapyrrole-triggered plastid signalling pathway integrates with the circadian clock in order to fine-tune nuclear gene expression during photoperiodic conditions. These findings provide novel insight into how clock components and plastid signals converge in order to obtain the proper output. I have also examined the regulation of nuclear gene expression in response to redox and early-light signals by identifying transcription factors responding to these signals. My work demonstrates a novel mechanism by which redox-regulation of specific transcription factors directly links cellular redox status to gene regulation. The identified transcription factors were further shown to regulate nuclear genes encoding plastid proteins and they are of particular importance for anterograde control during the early light response and establishment of photomorphogenic growth.

Place, publisher, year, edition, pages
Umeå: Umeå University , 2016. , 100 p.
Keyword [en]
Arabidopsis thaliana, chloroplast, cellular communication, tetrapyrrole, circadian clock, oxidative stress, light signalling, gene regulation
National Category
Biochemistry and Molecular Biology
Research subject
Molecular Biology
Identifiers
URN: urn:nbn:se:umu:diva-125373ISBN: 978-91-7601-550-6OAI: oai:DiVA.org:umu-125373DiVA: diva2:967708
Public defence
2016-10-06, KB3A9, KBC-huset, Umeå, 10:00 (English)
Opponent
Supervisors
Available from: 2016-09-15 Created: 2016-09-09 Last updated: 2016-09-15Bibliographically approved
List of papers
1. Interplay between HEAT SHOCK PROTEIN 90 and HY5 Controls PhANG expression in response to the GUN5 Plastid Signal
Open this publication in new window or tab >>Interplay between HEAT SHOCK PROTEIN 90 and HY5 Controls PhANG expression in response to the GUN5 Plastid Signal
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2012 (English)In: Molecular Plant, ISSN 1674-2052, E-ISSN 1752-9867, Vol. 5, no 4, 901-913 p.Article in journal (Refereed) Published
Abstract [en]

The presence of genes encoding organellar proteins in different cellular compartments necessitates a tight coordination of expression by the different genomes of the eukaryotic cell. This coordination of gene expression is achieved by organelle-to-nucleus or retrograde communication. Stress-induced perturbations of the tetrapyrrole pathway trigger large changes in nuclear gene expression in plants. Recently, we identified HSP90 proteins as ligands of the putative plastid signal Mg-ProtoIX. In order to investigate whether the interaction between HSP90 and Mg-ProtoIX is biologically relevant, we produced transgenic lines with reduced levels of cytosolic HSP90 in wild-type and gun5 backgrounds. Our work reveals that HSP90 proteins respond to the tetrapyrrole-mediated plastid signal to control expression of photosynthesis-associated nuclear genes (PhANG) during the response to oxidative stress. We also show that the hy5 mutant is insensitive to tetrapyrrole accumulation and that Mg-ProtoIX, cytosolic HSP90, and HY5 are all part of the same signaling pathway. These findings suggest that a regulatory complex controlling gene expression that includes HSP90 proteins and a transcription factor that is modified by tetrapyrroles in response to changes in the environment is evolutionarily conserved between yeast and plants.

Place, publisher, year, edition, pages
Oxford University Press, 2012
Keyword
abiotic/environmental stress, cell signaling, organelle biogenesis/function
National Category
Botany
Research subject
Physiological Botany
Identifiers
urn:nbn:se:umu:diva-60509 (URN)10.1093/mp/ssr112 (DOI)000306668400014 ()
External cooperation:
Available from: 2012-10-17 Created: 2012-10-15 Last updated: 2016-09-15Bibliographically approved
2. Circadian and Plastid Signaling Pathways Are Integrated to Ensure Correct Expression of the CBF and COR Genes during Photoperiodic Growth
Open this publication in new window or tab >>Circadian and Plastid Signaling Pathways Are Integrated to Ensure Correct Expression of the CBF and COR Genes during Photoperiodic Growth
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2016 (English)In: Plant Physiology, ISSN 0032-0889, E-ISSN 1532-2548, Vol. 171, no 2, 1392-1406 p.Article in journal (Refereed) Published
Abstract [en]

The circadian clock synchronizes a wide range of biological processes with the day/night cycle, and correct circadian regulation is essential for photosynthetic activity and plant growth. We describe here a mechanism where a plastid signal converges with the circadian clock to fine-tune the regulation of nuclear gene expression in Arabidopsis (Arabidopsis thaliana). Diurnal oscillations of tetrapyrrole levels in the chloroplasts contribute to the regulation of the nucleus-encoded transcription factors C-REPEAT BINDING FACTORS (CBFs). The plastid signal triggered by tetrapyrrole accumulation inhibits the activity of cytosolic HEAT SHOCK PROTEIN90 and, as a consequence, the maturation and stability of the clock component ZEITLUPE (ZTL). ZTL negatively regulates the transcription factor LONG HYPOCOTYL5 (HY5) and PSEUDO-RESPONSE REGULATOR5 (PRR5). Thus, low levels of ZTL result in a HY5- and PRR5-mediated repression of CBF3 and PRR5-mediated repression of CBF1 and CBF2 expression. The plastid signal thereby contributes to the rhythm of CBF expression and the downstream COLD RESPONSIVE expression during day/night cycles. These findings provide insight into how plastid signals converge with, and impact upon, the activity of well-defined clock components involved in circadian regulation.

National Category
Botany
Identifiers
urn:nbn:se:umu:diva-125464 (URN)10.1104/pp.16.00374 (DOI)000380699200048 ()27208227 (PubMedID)
External cooperation:
Available from: 2016-09-12 Created: 2016-09-12 Last updated: 2016-09-13Bibliographically approved
3. Redox-mediated Mechanisms Regulate DNA Binding Activity of the G-group of Basic Region Leucine Zipper (bZIP) Transcription Factors in Arabidopsis
Open this publication in new window or tab >>Redox-mediated Mechanisms Regulate DNA Binding Activity of the G-group of Basic Region Leucine Zipper (bZIP) Transcription Factors in Arabidopsis
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2012 (English)In: Journal of Biological Chemistry, ISSN 0021-9258, E-ISSN 1083-351X, Vol. 287, no 33, 27510-27525 p.Article in journal (Refereed) Published
Abstract [en]

Plant genes that contain the G-box in their promoters are responsive to a variety of environmental stimuli. Bioinformatics analysis of transcriptome data revealed that the G-box element is significantly enriched in promoters of high light-responsive genes. From nuclear extracts of high light-treated Arabidopsis plants, we identified the AtbZIP16 transcription factor as a component binding to the G-box-containing promoter fragment of light-harvesting chlorophyll a/b-binding protein2.4 (LHCB2.4). AtbZIP16 belongs to the G-group of Arabidopsis basic region leucine zipper (bZIP) type transcription factors. Although AtbZIP16 and its close homologues AtbZIP68 and AtGBF1 bind the G-box, they do not bind the mutated half-sites of the G-box palindrome. In addition, AtbZIP16 interacts with AtbZIP68 and AtGBF1 in the yeast two-hybrid system. A conserved Cys residue was shown to be necessary for redox regulation and enhancement of DNA binding activity in all three proteins. Furthermore, transgenic Arabidopsis lines overexpressing the wild type version of bZIP16 and T-DNA insertion mutants for bZIP68 and GBF1 demonstrated impaired regulation of LHCB2.4 expression. Finally, overexpression lines for the mutated Cys variant of bZIP16 provided support for the biological significance of Cys330 in redox regulation of gene expression. Thus, our results suggest that environmentally induced changes in the redox state regulate the activity of members of the G-group of bZIP transcription factors.

Place, publisher, year, edition, pages
Rockville: The American Society for Biochemistry and Molecular Biology, 2012
National Category
Biochemistry and Molecular Biology
Identifiers
urn:nbn:se:umu:diva-61574 (URN)10.1074/jbc.M112.361394 (DOI)000307840700027 ()
External cooperation:
Available from: 2012-11-27 Created: 2012-11-20 Last updated: 2016-09-12Bibliographically approved
4. The role of bZIP16, bZIP68 and GBF1 in early light response
Open this publication in new window or tab >>The role of bZIP16, bZIP68 and GBF1 in early light response
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(English)Manuscript (preprint) (Other academic)
National Category
Botany
Identifiers
urn:nbn:se:umu:diva-125471 (URN)
External cooperation:
Available from: 2016-09-12 Created: 2016-09-12 Last updated: 2016-09-12

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