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The chloroplast talks: Insights into the language of the chloroplast in Arabidopsis
Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC). (Åsa Strand)
2010 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

The chloroplast originates from an endosymbiotic event 1.5 billion years ago, when a free living photosynthetic bacteria was engulfed by a eukaryotic host. The chloroplastic genome has through evolution lost many genes to the nuclear genome of the host. To coordinate the gene expression between the two genomes, plants have evolved two types of communication, nucleus-to-plastid (anterograde) and plastid-to-nucleus (retrograde) signalling. This thesis will focus on retrograde communication with emphasis on redox and tetrapyrrole mediated signalling.

In this thesis, we establish the tetrapyrrole Mg-ProtoIX as an important retrograde negative regulator of nuclear encoded plastid proteins. We show that Mg-ProtoIX accumulates in both artificial and natural stress conditions, and that the accumulation is tightly correlated to regulation of nuclear gene expression. Using confocal microscopy, we could visualize Mg-ProtoIX in the cytosol during stress conditions. In addition, exogenously applied Mg-ProtoIX stayed in the cytosol and was enough to trigger a signal to the nucleus. The results presented here indicate that Mg-ProtoIX is transported out of the chloroplast to control nuclear gene expression. Mg-ProtoIX mediated repression of the nuclear gene, COR15a, occurs via the transcription factor HY5. HY5 is influenced by both plastid signals and the photoreceptors. Here, we show that photoreceptors are part of Mg-ProtoIX mediated signalling as well as excess light adaptation. We identified the blue light receptor, CRY1, as a light intensity sensor that partly utilizes HY5 in the high light response. To further understand the high light regulation of nuclear genes, we isolated a mutant with redox insensitive (rin) high light response. The rin2 mutant has a mutated plastid protein with unknown function. Characterization of the rin2 mutant revealed that the protein is important in regulating plastid gene expression as well as nuclear gene expression. The rin2 mutant is the first characterized rin mutant and could prove important in elucidating the cross-talk between redox mediated coordination between the plastid and the nuclear genome.

Place, publisher, year, edition, pages
Umeå: Department of Plant Physiology, Umeå Plant Science Centre, Umeå University , 2010. , 76 p.
Keyword [en]
Arabidopsis thaliana, chloroplast, photosynthesis, retrograde communication, Mg-ProtoIX, oxidative stress, gene expression
National Category
Biochemistry and Molecular Biology
Research subject
Physiological Botany
Identifiers
URN: urn:nbn:se:umu:diva-36166ISBN: 978-91-7459-069-2 (print)OAI: oai:DiVA.org:umu-36166DiVA: diva2:352462
Public defence
2010-10-15, KBC-huset, KB3A9, Umeå universitet, Umeå, 13:00 (English)
Opponent
Supervisors
Available from: 2010-09-24 Created: 2010-09-21 Last updated: 2015-05-06Bibliographically approved
List of papers
1. In vivo visualization of Mg-ProtoporphyrinIX, a coordinator of photosynthetic gene expression in the nucleus and the chloroplast
Open this publication in new window or tab >>In vivo visualization of Mg-ProtoporphyrinIX, a coordinator of photosynthetic gene expression in the nucleus and the chloroplast
2007 (English)In: Plant Cell, ISSN 1040-4651, Vol. 19, no 6, 1964-1979 p.Article in journal (Refereed) Published
Abstract [en]

The photosynthetic apparatus is composed of proteins encoded by genes from both the nucleus and the chloroplast. To ensure that the photosynthetic complexes are assembled stoichiometrically and to enable their rapid reorganization in response to a changing environment, the plastids emit signals that regulate nuclear gene expression to match the status of the plastids. One of the plastid signals, the chlorophyll intermediate Mg-ProtoporphyrinIX (Mg-ProtoIX) accumulates under stress conditions and acts as a negative regulator of photosynthetic gene expression. By taking advantage of the photoreactive property of tetrapyrroles, Mg-ProtoIX could be visualized in the cells using confocal laser scanning spectroscopy. Our results demonstrate that Mg-ProtoIX accumulated both in the chloroplast and in the cytosol during stress conditions. Thus, the signaling metabolite is exported from the chloroplast, transmitting the plastid signal to the cytosol. Our results from the Mg-ProtoIX over- and underaccumulating mutants copper response defect and genome uncoupled5, respectively, demonstrate that the expression of both nuclear- and plastid-encoded photosynthesis genes is regulated by the accumulation of Mg-ProtoIX. Thus, stress-induced accumulation of the signaling metabolite Mg-ProtoIX coordinates nuclear and plastidic photosynthetic gene expression.

Place, publisher, year, edition, pages
Rockville Pike, Bethesda MD, USA: National Center for Biotechnology Information, U.S. National Library of Medicine, 2007
Identifiers
urn:nbn:se:umu:diva-15860 (URN)doi:10.1105/tpc.106.048744 (DOI)17586657 (PubMedID)
Available from: 2007-08-03 Created: 2007-08-03 Last updated: 2015-05-06Bibliographically approved
2. Interaction between Mg-protoporphyrin IX and HEAT SHOCK PROTEIN 81 is essential for regulation of LHCB expression during plant stress response:
Open this publication in new window or tab >>Interaction between Mg-protoporphyrin IX and HEAT SHOCK PROTEIN 81 is essential for regulation of LHCB expression during plant stress response:
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2010 (English)Manuscript (preprint) (Other academic)
Publisher
213 p.
Identifiers
urn:nbn:se:umu:diva-36162 (URN)987-91-7459-069-2 (ISBN)
Available from: 2010-09-21 Created: 2010-09-21 Last updated: 2015-05-06Bibliographically approved
3. Expression of COR15a is regulated by an interplay between tetrapyrrole accumulation and HY5 in Arabidopsis thaliana
Open this publication in new window or tab >>Expression of COR15a is regulated by an interplay between tetrapyrrole accumulation and HY5 in Arabidopsis thaliana
(English)Manuscript (preprint) (Other academic)
Identifiers
urn:nbn:se:umu:diva-36164 (URN)
Available from: 2010-09-21 Created: 2010-09-21 Last updated: 2015-05-06Bibliographically approved
4. Genome-wide gene expression analysis reveals a critical role for CRYPTOCHROME1 in the response of Arabidopsis to high irradiance
Open this publication in new window or tab >>Genome-wide gene expression analysis reveals a critical role for CRYPTOCHROME1 in the response of Arabidopsis to high irradiance
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2007 (English)In: Plant Physiology, ISSN 0032-0889, Vol. 144, no 3, 1391-406 p.Article in journal (Refereed) Published
Abstract [en]

Exposure to high irradiance results in dramatic changes in nuclear gene expression in plants. However, little is known about the mechanisms by which changes in irradiance are sensed and how the information is transduced to the nucleus to initiate the genetic response. To investigate whether the photoreceptors are involved in the response to high irradiance, we analyzed expression of EARLY LIGHT-INDUCIBLE PROTEIN1 (ELIP1), ELIP2, ASCORBATE PEROXIDASE2 (APX2), and LIGHT-HARVESTING CHLOROPHYLL A/B-BINDING PROTEIN2.4 (LHCB2.4) in the phytochrome A (phyA), phyB, cryptochrome1 (cry1), and cry2 photoreceptor mutants and long hypocotyl5 (hy5) and HY5 homolog (hyh) transcription factor mutants. Following exposure to high intensity white light for 3 h (1,000 µmol quanta m–2 s–1) expression of ELIP1/2 and APX2 was strongly induced and LHCB2.4 expression repressed in wild type. The cry1 and hy5 mutants showed specific misregulation of ELIP1/2, and we show that the induction of ELIP1/2 expression is mediated via CRY1 in a blue light intensity-dependent manner. Furthermore, using the Affymetrix Arabidopsis (Arabidopsis thaliana) 24 K Gene-Chip, we showed that 77 of the high light-responsive genes are regulated via CRY1, and 26 of those genes were also HY5 dependent. As a consequence of the misregulation of these genes, the cry1 mutant displayed a high irradiance-sensitive phenotype with significant photoinactivation of photosystem II, indicated by reduced maximal fluorescence ratio. Thus, we describe a novel function of CRY1 in mediating plant responses to high irradiances that is essential to the induction of photoprotective mechanisms. This indicates that high irradiance can be sensed in a chloroplast-independent manner by a cytosolic/nucleic component.

Identifiers
urn:nbn:se:umu:diva-15861 (URN)doi:10.1104/pp.107.098293 (DOI)17478635 (PubMedID)
Available from: 2007-08-03 Created: 2007-08-03 Last updated: 2015-05-06Bibliographically approved
5. RIN2, a novel chloroplast protein involved in retrograde signaling in response to excess light
Open this publication in new window or tab >>RIN2, a novel chloroplast protein involved in retrograde signaling in response to excess light
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(English)Manuscript (preprint) (Other academic)
National Category
Biological Sciences
Identifiers
urn:nbn:se:umu:diva-36165 (URN)
Available from: 2010-09-21 Created: 2010-09-21 Last updated: 2015-05-06Bibliographically approved

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