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  • 1. Ankele, Elisabeth
    et al.
    Kindgren, Peter
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Pesquet, Edouard
    Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC). Umeå University, Faculty of Science and Technology, Department of Plant Physiology.
    Strand, Åsa
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    In vivo visualization of Mg-ProtoporphyrinIX, a coordinator of photosynthetic gene expression in the nucleus and the chloroplast2007In: Plant Cell, ISSN 1040-4651, Vol. 19, no 6, p. 1964-1979Article in journal (Refereed)
    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.

  • 2.
    Kindgren, Peter
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    The chloroplast talks: Insights into the language of the chloroplast in Arabidopsis2010Doctoral 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.

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  • 3.
    Kindgren, Peter
    et al.
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology.
    Barajas López, Juan de Dios
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology.
    Shaikhali, Jehad
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology.
    Benedict, Catherine
    Mohapatra, Anasuya
    Gough, Simon P.
    Hansson, Mats
    Kieselbach, Thomas
    Umeå University, Faculty of Science and Technology, Department of Chemistry.
    Strand, Åsa
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology.
    Interaction between Mg-protoporphyrin IX and HEAT SHOCK PROTEIN 81 is essential for regulation of LHCB expression during plant stress response: 2010Manuscript (preprint) (Other academic)
  • 4.
    Kindgren, Peter
    et al.
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Dubreuil, Carole
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Strand, Åsa
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    The Recovery of Plastid Function Is Required for Optimal Response to Low Temperatures in Arabidopsis2015In: PLoS ONE, ISSN 1932-6203, E-ISSN 1932-6203, Vol. 10, no 9, article id e0138010Article in journal (Refereed)
    Abstract [en]

    Cold acclimation is an essential response in higher plants to survive freezing temperatures. Here, we report that two independent mutant alleles of the H-subunit of Mg-chelatase, CHLH, gun5-1 and cch in Arabidopsis are sensitive to low temperatures. Plants were grown in photoperiodic conditions and exposed to low temperatures for short-and long-term periods. Tetrapyrrole biosynthesis was initially significantly inhibited in response to low temperature but recovered in wild type (Col-0), although the tetrapyrrole levels were lower in cold compared to control conditions. The gun5-1 and cch alleles showed an inability to recover chlorophyll biosynthesis in addition to a significant decrease in freezing tolerance. We found that the impaired plastid function in the CHLH mutant plants resulted in compromised de novo protein synthesis at low temperatures. The expression of the transcription factors CBF1-3 was super-induced in gun5-1 and cch mutant alleles but expression levels of their target genes, COR15a, COR47 and COR78 were similar or even lower compared to Col-0. In addition, the protein levels of COR15a were lower in gun5-1 and cch and a general defect in protein synthesis could be seen in the gun5-1 mutant following a 35S labelling experiment performed at low temperature. Taken together, our results demonstrate the importance of a functional chloroplast for the cold acclimation process and further suggest that impaired plastid function could result in inhibition of protein synthesis at low temperature.

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  • 5.
    Kindgren, Peter
    et al.
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Eriksson, Mats-Jerry
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Benedict, Catherine
    Mohapatra, Anasuya
    Gough, Simon P
    Carlsberg Laboratory, 2500 Copenhagen Valby, Denmark.
    Hansson, Mats
    Carlsberg Laboratory, 2500 Copenhagen Valby, Denmark.
    Kieselbach, Thomas
    Umeå University, Faculty of Science and Technology, Department of Chemistry.
    Strand, Åsa
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    A novel proteomic approach reveals a role for Mg-protoporphyrin IX in response to oxidative stress2011In: Physiologia Plantarum: An International Journal for Plant Biology, ISSN 0031-9317, E-ISSN 1399-3054, Vol. 141, no 4, p. 310-320Article in journal (Refereed)
    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 communication. Stress-induced perturbations of the tetrapyrrole pathway trigger large changes in nuclear gene expression. In order to investigate whether the tetrapyrrole Mg-ProtoIX itself is an important part of plastid-to-nucleus communication, we used an affinity column containing Mg-ProtoIX covalently linked to an Affi-Gel matrix. The proteins that bound to Mg-ProtoIX were analyzed by sodium dodecyl sulfate polyacrylamide gel electrophoresis combined with nano liquid chromatography–mass spectrometry (MS)/MS. Thus, we present a novel proteomic approach to address the mechanisms involved in cellular signaling and we identified interactions between Mg-ProtoIX and a large number of proteins associated with oxidative stress responses. Our approach revealed an interaction between Mg-ProtoIX and the heat shock protein 90-type protein, HSP81-2 suggesting that a regulatory complex including HSP90 proteins and tetrapyrroles controlling gene expression is evolutionarily conserved between yeast and plants. In addition, our list of putative Mg-ProtoIX-binding proteins demonstrated that binding of tetrapyrroles does not depend on a specific amino acid motif but possibly on a specific fold of the protein.

  • 6.
    Kindgren, Peter
    et al.
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Kremnev, Dmitry
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Barajas López, Juan de Dios
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Eriksson, Mats-Jerry
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Tellgren-Roth, Christian
    Department of Genetics and Pathology, Rudbecklaboratoriet, Uppsala University.
    Kleine, Tatjana
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Small, Ian D
    The University of Western Australia, 35 Stirling Highway Crawley 6009 WA, Australia.
    Strand, Åsa
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    RIN2, a novel chloroplast protein involved in retrograde signaling in response to excess lightManuscript (preprint) (Other academic)
  • 7.
    Kindgren, Peter
    et al.
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Kremnev, Dmitry
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Blanco, Nicolas E.
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Lopez, Juan de Dios Barajas
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Fernandez, Aurora Pinas
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Tellgren-Roth, Christian
    Uppsala Univ, Rudbecklab, Dept Immunol Genet & Pathol, S-75185 Uppsala, Sweden.
    Kleine, Tatjana
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Small, Ian
    Univ Western Australia, Australian Res Council Ctr Excellence Plant Energ, Nedlands, WA 6009, Australia.
    Strand, Åsa
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    The plastid redox insensitive 2 mutant of Arabidopsis is impaired in PEP activity and high light-dependent plastid redox signalling to the nucleus2012In: The Plant Journal, ISSN 0960-7412, E-ISSN 1365-313X, Vol. 70, no 2, p. 279-291Article in journal (Refereed)
    Abstract [en]

    The photosynthetic apparatus is composed of proteins encoded by genes from both the nuclear and the chloroplastic genomes. The activities of the nuclear and chloroplast genomes must therefore be closely coordinated through intracellular signalling. The plastids produce multiple retrograde signals at different times of their development, and in response to changes in the environment. These signals regulate the expression of nuclear-encoded photosynthesis genes to match the current status of the plastids. Using forward genetics we identified PLASTID REDOX INSENSITIVE 2 (PRIN2), a chloroplast component involved in redox-mediated retrograde signalling. The allelic mutants prin2-1 and prin2-2 demonstrated a misregulation of photosynthesis-associated nuclear gene expression in response to excess light, and an inhibition of photosynthetic electron transport. As a consequence of the misregulation of LHCB1.1 and LHCB2.4, the prin2 mutants displayed a high irradiance-sensitive phenotype with significant photoinactivation of photosystem II, indicated by a reduced variable to maximal fluorescence ratio (Fv/Fm). PRIN2 is localized to the nucleoids, and plastid transcriptome analyses demonstrated that PRIN2 is required for full expression of genes transcribed by the plastid-encoded RNA polymerase (PEP). Similarly to the prin2 mutants, the ys1 mutant with impaired PEP activity also demonstrated a misregulation of LHCB1.1 and LHCB2.4 expression in response to excess light, suggesting a direct role for PEP activity in redox-mediated retrograde signalling. Taken together, our results indicate that PRIN2 is part of the PEP machinery, and that the PEP complex responds to photosynthetic electron transport and generates a retrograde signal, enabling the plant to synchronize the expression of photosynthetic genes from both the nuclear and plastidic genomes.

  • 8.
    Kindgren, Peter
    et al.
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology.
    Mats-Jerry, Eriksson
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology.
    Strand, Åsa
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology.
    Expression of COR15a is regulated by an interplay between tetrapyrrole accumulation and HY5 in Arabidopsis thalianaManuscript (preprint) (Other academic)
  • 9.
    Kindgren, Peter
    et al.
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Norén, Louise
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Barajas Lopez, Juan de Dios
    Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC). Umeå University, Faculty of Science and Technology, Department of Plant Physiology.
    Shaikhali, Jehad
    Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC). Umeå University, Faculty of Science and Technology, Department of Plant Physiology.
    Strand, Åsa
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Interplay between HEAT SHOCK PROTEIN 90 and HY5 Controls PhANG expression in response to the GUN5 Plastid Signal2012In: Molecular Plant, ISSN 1674-2052, E-ISSN 1752-9867, Vol. 5, no 4, p. 901-913Article in journal (Refereed)
    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.

  • 10.
    Kindgren, Peter
    et al.
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Strand, Åsa
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Chloroplast transcription, untangling the Gordian Knot2015In: New Phytologist, ISSN 0028-646X, E-ISSN 1469-8137, Vol. 206, no 3, p. 889-891Article in journal (Other academic)
  • 11. Kleine, Tatjana
    et al.
    Kindgren, Peter
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Benedict, Catherine
    Hendrickson, Luke
    Strand, Åsa
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Genome-wide gene expression analysis reveals a critical role for CRYPTOCHROME1 in the response of Arabidopsis to high irradiance2007In: Plant Physiology, ISSN 0032-0889, Vol. 144, no 3, p. 1391-406Article in journal (Refereed)
    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.

  • 12.
    Norén, Louise
    et al.
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Kindgren, Peter
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC). Copenhagen Plant Science Centre, University of Copenhagen.
    Stachula, Paulina
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Rühl, Mark
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Eriksson, Maria E.
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Hurry, Vaughan
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Strand, Åsa
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Circadian and Plastid Signaling Pathways Are Integrated to Ensure Correct Expression of the CBF and COR Genes during Photoperiodic Growth2016In: Plant Physiology, ISSN 0032-0889, E-ISSN 1532-2548, Vol. 171, no 2, p. 1392-1406Article in journal (Refereed)
    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.

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