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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. Barajas-Lopez, Juan de Dios
    et al.
    Blanco, Nicolas E.
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology.
    Strand, Åsa
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology.
    Plastid-to-nucleus communication, signals controlling the running of the plant cell2013In: Biochimica et Biophysica Acta. Molecular Cell Research, ISSN 0167-4889, E-ISSN 1879-2596, Vol. 1833, no 2, p. 425-437Article, review/survey (Refereed)
    Abstract [en]

    The presence of genes encoding organellar proteins in both the nucleus and the organelle necessitates tight coordination of expression by the different genomes, and this has led to the evolution of sophisticated intracellular signaling networks. Organelle-to-nucleus signaling, or retrograde control, coordinates the expression of nuclear genes encoding organellar proteins with the metabolic and developmental state of the organelle. Complex networks of retrograde signals orchestrate major changes in nuclear gene expression and coordinate cellular activities and assist the cell during plant development and stress responses. It has become clear that, even though the chloroplast depends on the nucleus for its function, plastid signals play important roles in an array of different cellular processes vital to the plant. Hence, the chloroplast exerts significant control over the running of the cell. This article is part of a Special Issue entitled: Protein Import and Quality Control in Mitochondria and Plastids. 

  • 3.
    Barajas-Lopez, Juan de Dios
    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).
    Shaikhali, Jehad
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Pinas-Fernandez, Aurora
    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).
    PAPP5 is involved in the tetrapyrrole mediated plastid signalling during chloroplast development2013In: PLoS ONE, ISSN 1932-6203, E-ISSN 1932-6203, Vol. 8, no 3, article id e60305Article in journal (Refereed)
    Abstract [en]

    The initiation of chloroplast development in the light is dependent on nuclear encoded components. The nuclear genes encoding key components in the photosynthetic machinery are regulated by signals originating in the plastids. These plastid signals play an essential role in the regulation of photosynthesis associated nuclear genes (PhANGs) when proplastids develop into chloroplasts. One of the plastid signals is linked to the tetrapyrrole biosynthesis and accumulation of the intermediates the Mg-ProtoIX and its methyl ester Mg-ProtoIX-ME. Phytochrome-Associated Protein Phosphatase 5 (PAPP5) was isolated in a previous study as a putative Mg-ProtoIX interacting protein. In order to elucidate if there is a biological link between PAPP5 and the tetrapyrrole mediated signal we generated double mutants between the Arabidopsis papp5 and the crd mutants. The crd mutant over-accumulates Mg-ProtoIX and Mg-ProtoIX-ME and the tetrapyrrole accumulation triggers retrograde signalling. The crd mutant exhibits repression of PhANG expression, altered chloroplast morphology and a pale phenotype. However, in the papp5crd double mutant, the crd phenotype is restored and papp5crd accumulated wild type levels of chlorophyll, developed proper chloroplasts and showed normal induction of PhANG expression in response to light. Tetrapyrrole feeding experiments showed that PAPP5 is required to respond correctly to accumulation of tetrapyrroles in the cell and that PAPP5 is most likely a component in the plastid signalling pathway down stream of the tetrapyrrole Mg-ProtoIX/Mg-ProtoIX-ME. Inhibition of phosphatase activity phenocopied the papp5crd phenotype in the crd single mutant demonstrating that PAPP5 phosphatase activity is essential to mediate the retrograde signal and to suppress PhANG expression in the crd mutant. Thus, our results suggest that PAPP5 receives an inbalance in the tetrapyrrole biosynthesis through the accumulation of Mg-ProtoIX and acts as a negative regulator of PhANG expression during chloroplast biogenesis and development.

  • 4.
    Blanco, Nicolas E.
    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).
    Guinea-Diaz, Manuel
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Whelan, James
    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).
    Interaction between plastid and mitochondrial retrograde signalling pathways during changes to plastid redox status2014In: Philosophical Transactions of the Royal Society of London. Biological Sciences, ISSN 0962-8436, E-ISSN 1471-2970, Vol. 369, no 1640, article id 20130231Article in journal (Refereed)
    Abstract [en]

    Mitochondria and chloroplasts depend upon each other; photosynthesis provides substrates for mitochondrial respiration and mitochondrial metabolism is essential for sustaining photosynthetic carbon assimilation. In addition, mitochondrial respiration protects photosynthesis against photoinhibition by dissipating excess redox equivalents from the chloroplasts. Genetic defects in mitochondrial function result in an excessive reduction and energization of the chloroplast. Thus, it is clear that the activities of mitochondria and plastids need to be coordinated, but the manner by which the organelles communicate to coordinate their activities is unknown. The regulator of alternative oxidase (rao1) mutant was isolated as a mutant unable to induce AOX1a expression in response to the inhibitor of the mitochondrial cytochrome c reductase (complex III), antimycin A. RAO1 encodes the nuclear localized cyclin-dependent kinase E1 (CDKE1). Interestingly, the rao1 mutant demonstrates a genome uncoupled phenotype also in response to redox changes in the photosynthetic electron transport chain. Thus, CDKE1 was shown to regulate both LIGHT HARVESTING COMPLEX B (LHCB) and ALTERNATIVE OXIDASE 1 (AOX1a) expression in response to retrograde signals. Our results suggest that CDKE1 is a central nuclear component integrating mitochondrial and plastid retrograde signals and plays a role in regulating energy metabolism during the response to stress.

  • 5.
    Blanco, Nicolas E.
    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). Centro de Estudios Fotosintéticos y Bioquímicos, Universidad Nacional de Rosario (CEFOBI-CONICET/UNR), Rosario, Argentina.
    Liebsch, Daniela
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC). Instituto de Biología Molecular y Celular de Rosario (IBR-CONICET), Rosario, Argentina.
    Guinea Diaz, Manuel
    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).
    Whelan, James
    Dual and dynamic intracellular localization of Arabidopsis thaliana SnRK1.12019In: Journal of Experimental Botany, ISSN 0022-0957, E-ISSN 1460-2431, Vol. 70, no 8, p. 2325-2338Article in journal (Refereed)
    Abstract [en]

    Sucrose non-fermenting 1 (SNF1)-related protein kinase 1.1 (SnRK1.1; also known as KIN10 or SnRK1 alpha) has been identified as the catalytic subunit of the complex SnRK1, the Arabidopsis thaliana homologue of a central integrator of energy and stress signalling in eukaryotes dubbed AMPK/Snf1/SnRK1. A nuclear localization of SnRK1.1 has been previously described and is in line with its function as an integrator of energy and stress signals. Here, using two biological models (Nicotiana benthamiana and Arabidopsis thaliana), native regulatory sequences, different microscopy techniques, and manipulations of cellular energy status, it was found that SnRK1.1 is localized dynamically between the nucleus and endoplasmic reticulum (ER). This distribution was confirmed at a spatial and temporal level by co-localization studies with two different fluorescent ER markers, one of them being the SnRK1.1 phosphorylation target HMGR. The ER and nuclear localization displayed a dynamic behaviour in response to perturbations of the plastidic electron transport chain. These results suggest that an ER-associated SnRK1.1 fraction might be sensing the cellular energy status, being a point of crosstalk with other ER stress regulatory pathways.

  • 6.
    Dubreuil, Carole
    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).
    Ji, Yan
    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).
    Grönlund, Andreas
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    A quantitative model of the phytochrome-PIF light signalling initiating chloroplast development2017In: Scientific Reports, ISSN 2045-2322, E-ISSN 2045-2322, Vol. 7, article id 13884Article in journal (Refereed)
    Abstract [en]

    The components required for photosynthesis are encoded in two separate genomes, the nuclear and the plastid. To address how synchronization of the two genomes involved can be attained in early light-signalling during chloroplast development we have formulated and experimentally tested a mathematical model simulating light sensing and the following signalling response. The model includes phytochrome B (PhyB), the phytochrome interacting factor 3 (PIF3) and putative regulatory targets of PIF3. Closed expressions of the phyB and PIF3 concentrations after light exposure are derived, which capture the relevant timescales in the response of genes regulated by PIF3. Sequence analysis demonstrated that the promoters of the nuclear genes encoding sigma factors (SIGs) and polymerase-associated proteins (PAPs) required for expression of plastid encoded genes, contain the cis-elements for binding of PIF3. The model suggests a direct link between light inputs via PhyB-PIF3 to the plastid transcription machinery and control over the expression of photosynthesis components both in the nucleus and in the plastids. Using a pluripotent Arabidopsis cell culture in which chloroplasts develop from undifferentiated proplastids following exposure to light, we could experimentally verify that the expression of SIGs and PAPs in response to light follow the calculated expression of a PhyB-PIF3 regulated gene.

  • 7.
    Dubreuil, Carole
    et al.
    Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC). Umeå University, Faculty of Science and Technology, Department of Plant Physiology.
    Jin, Xu
    Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC). Umeå University, Faculty of Science and Technology, Department of Plant Physiology.
    Barajas-López, 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.
    Hewitt, Timothy C.
    Tanz, Sandra K.
    Dobrenel, Thomas
    Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC). Umeå University, Faculty of Science and Technology, Department of Plant Physiology.
    Schröder, Wolfgang P.
    Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC). Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Department of Chemistry.
    Hanson, Johannes
    Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC). Umeå University, Faculty of Science and Technology, Department of Plant Physiology.
    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. Arrhenius Laboratory, Department of Ecology, Environment, and Plant Sciences, Stockholm University, SE-106 91 Stockholm, Sweden.
    Grönlund, Andreas
    Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC). Umeå University, Faculty of Science and Technology, Department of Plant Physiology.
    Small, Ian
    Strand, Åsa
    Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC). Umeå University, Faculty of Science and Technology, Department of Plant Physiology.
    Establishment of Photosynthesis through Chloroplast Development Is Controlled by Two Distinct Regulatory Phases2018In: Plant Physiology, ISSN 0032-0889, E-ISSN 1532-2548, Vol. 176, no 2, p. 1199-1214Article in journal (Refereed)
    Abstract [en]

    Chloroplasts develop from undifferentiated proplastids present in meristematic tissue. Thus, chloroplast biogenesis is closely connected to leaf development, which restricts our ability to study the process of chloroplast biogenesis per se. As a consequence, we know relatively little about the regulatory mechanisms behind the establishment of the photosynthetic reactions and how the activities of the two genomes involved are coordinated during chloroplast development. We developed a single cell-based experimental system from Arabidopsis (Arabidopsis thaliana) with high temporal resolution allowing for investigations of the transition from proplastids to functional chloroplasts. Using this unique cell line, we could show that the establishment of photosynthesis is dependent on a regulatory mechanism involving two distinct phases. The first phase is triggered by rapid light-induced changes in gene expression and the metabolome. The second phase is dependent on the activation of the chloroplast and generates massive changes in the nuclear gene expression required for the transition to photosynthetically functional chloroplasts. The second phase also is associated with a spatial transition of the chloroplasts from clusters around the nucleus to the final position at the cell cortex. Thus, the establishment of photosynthesis is a two-phase process with a clear checkpoint associated with the second regulatory phase allowing coordination of the activities of the nuclear and plastid genomes.

  • 8.
    Ganeteg, U.
    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).
    Gustafsson, P.
    Jansson, S.
    The properties of the chlorophyll a/b-binding proteins Lhca2 and Lhca3 studied in vivo using antisense inhibition2001In: Plant Physiol, Vol. 127, p. 150-158Article in journal (Refereed)
  • 9.
    Guinea Diaz, Manuel
    et al.
    Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Hernandez-Verdeja, Tamara
    Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Kremnev, Dmitry
    Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Crawford, Tim
    Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Dubreuil, Carole
    Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Strand, Åsa
    Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Redox regulation of PEP activity during seedling establishment in Arabidopsis thaliana2018In: Nature Communications, ISSN 2041-1723, E-ISSN 2041-1723, Vol. 9, article id 50Article in journal (Refereed)
    Abstract [en]

    Activation of the plastid-encoded RNA polymerase is tightly controlled and involves a network of phosphorylation and, as yet unidentified, thiol-mediated events. Here, we characterize PLASTID REDOX INSENSITIVE2, a redox-regulated protein required for full PEP-driven transcription. PRIN2 dimers can be reduced into the active monomeric form by thioredoxins through reduction of a disulfide bond. Exposure to light increases the ratio between the monomeric and dimeric forms of PRIN2. Complementation of prin2-2 with different PRIN2 protein variants demonstrates that the monomer is required for light-activated PEP-dependent transcription and that expression of the nuclear-encoded photosynthesis genes is linked to the activity of PEP. Activation of PEP during chloroplast development likely is the source of a retrograde signal that promotes nuclear LHCB expression. Thus, regulation of PRIN2 is the thiol-mediated mechanism required for full PEP activity, with PRIN2 monomerization via reduction by TRXs providing a mechanistic link between photosynthetic electron transport and activation of photosynthetic gene expression.

  • 10.
    Hernandez-Verdeja, Tamara
    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).
    Retrograde Signals Navigate the Path to Chloroplast Development2018In: Plant Physiology, ISSN 0032-0889, E-ISSN 1532-2548, Vol. 176, no 2, p. 967-976Article in journal (Refereed)
  • 11.
    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)
  • 12.
    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.

  • 13.
    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.

  • 14.
    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)
  • 15.
    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.

  • 16.
    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)
  • 17.
    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.

  • 18.
    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)
  • 19. 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.

  • 20.
    Kremnev, Dmitry
    et al.
    Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Guinea Diaz, Manuel
    Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Dubreuil, Carole
    Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Strand, Åsa
    Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Redox regulation of PEP activity during seedling development in ArabidopsisManuscript (preprint) (Other academic)
  • 21.
    Kremnev, Dmitry
    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).
    Plastid encoded RNA polymerase activity and expression of photosynthesis genes required for embryo and seed development in Arabidopsis2014In: Frontiers in Plant Science, ISSN 1664-462X, E-ISSN 1664-462XArticle in journal (Refereed)
    Abstract [en]

    Chloroplast biogenesis and function is essential for proper plant embryo and seed development but the molecular mechanisms underlying the role of plastids during embryogenesis are poorly understood. Expression of plastid encoded genes is dependent on two different transcription machineries; a plastid-encoded bacterial-type RNA polymerase (PEP) and a nuclear-encoded phage-type RNA polymerase (NEP), which recognize distinct types of promoters. However, the division of labor between PEP and NEP during plastid development and in mature chloroplasts is unclear. We show here that PLASTID REDOX INSENSITIVE 2 (PRIN2) and CHLOROPLAST STEM-LOOP BINDING PROTEIN 41 kDa (CSP41b), two proteins identified in plastid nucleoid preparations, are essential for proper plant embryo development. Using Co-IP assays and native PAGE we have shown a direct physical interaction between PRIN2 and CSP41b. Moreover, PRIN2 and CSP41b form a distinct protein complex in vitro that binds DNA. The prin2.2 and csp41b-2 single mutants displayed pale phenotypes, abnormal chloroplasts with reduced transcript levels of photosynthesis genes and defects in embryo development. The respective csp41b-2prin2.2 homo/heterozygote double mutants produced abnormal white colored ovules and shrunken seeds. Thus, the csp41b-2prin2.2 double mutant is embryo lethal. In silico analysis of available array data showed that a large number of genes traditionally classified as PEP dependent genes are transcribed during early embryo development from the pre-globular stage to the mature-green-stage. Taken together, our results suggest that PEP activity and consequently the switch from NEP to PEP activity, is essential during embryo development and that the PRIN2-CSP41b DNA binding protein complex possibly is important for full PEP activity during this process.

  • 22. Ng, Sophia
    et al.
    Giraud, Estelle
    Duncan, Owen
    Law, Simon R.
    Wang, Yan
    Xu, Lin
    Narsai, Reena
    Carrie, Chris
    Walker, Hayden
    Day, David A.
    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).
    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).
    Whelan, James
    Ivanova, Aneta
    Cyclin-dependent Kinase E1 (CDKE1) Provides a Cellular Switch in Plants between Growth and Stress Responses2013In: Journal of Biological Chemistry, ISSN 0021-9258, E-ISSN 1083-351X, Vol. 288, no 5, p. 3449-3459Article in journal (Refereed)
    Abstract [en]

    Plants must deal effectively with unfavorable growth conditions that necessitate a coordinated response to integrate cellular signals with mitochondrial retrograde signals. A genetic screen was carried out to identify regulators of alternative oxidase (rao mutants), using AOX1a expression as a model system to study retrograde signaling in plants. Two independent rao1 mutant alleles identified CDKE1 as a central nuclear component integrating mitochondrial retrograde signals with energy signals under stress. CDKE1 is also necessary for responses to general cellular stresses, such as H2O2 and cold that act, at least in part, via anterograde pathways, and integrates signals from central energy/stress sensing kinase signal transduction pathways within the nucleus. Together, these results place CDKE1 as a central kinase integrating diverse cellular signals and shed light on a mechanism by which plants can effectively switch between growth and stress responses.

  • 23.
    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.

  • 24.
    Norén, Louise
    et al.
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology.
    Kindgren, Peter
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Copenhagen Plant Science Centre, University of Copenhagen, Thorvaldsenvej 40, 1871 Frederiksberg, Denmark.
    Stachula, Paulina
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology.
    Rühl, Mark
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology.
    Eriksson, Maria E.
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology.
    Hurry, Vaughan
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology.
    Strand, Åsa
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology.
    HSP90, ZTL, PRR5 and HY5 integrate circadian and plastid signaling pathways to regulate CBF and COR expressionManuscript (preprint) (Other academic)
  • 25.
    Piñas Fernández, Aurora
    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).
    Retrograde signaling and plant stress: plastid signals initiate cellular stress responses2008In: Current opinion in plant biology, ISSN 1369-5266, E-ISSN 1879-0356, Vol. 11, no 5, p. 509-513Article in journal (Refereed)
    Abstract [en]

    Retrograde signaling coordinates the expression of nuclear genes encoding organellar proteins with the metabolic and developmental state of the organelle. These plastid signals are essential not only for coordinating photosynthetic gene expression in both the nucleus and in the chloroplasts but also for mediating plant stress responses. The chloroplasts therefore act as sensors of environmental changes and complex networks of plastid signals coordinate cellular activities and assist the cell during plant stress responses. Recent work suggests that information from both cytosolic-signaling and plastid-signaling networks must be integrated for the plant cell to respond optimally to environmental stress.

  • 26.
    Razzak, Abdur
    et al.
    Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC). Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå Plant Science Centre, Department of Forest Genetics and Plant Physiology, Swedish University of Agricultural Sciences, Umeå SE-901 87, Sweden.
    Ranade, Sonali Sachin
    Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC). Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå Plant Science Centre, Department of Forest Genetics and Plant Physiology, Swedish University of Agricultural Sciences, Umeå SE-901 87, Sweden.
    Strand, Åsa
    Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC). Umeå University, Faculty of Science and Technology, Department of Plant Physiology.
    Garcia-Gil, M. R.
    Differential response of Scots pine seedlings to variable intensity and ratio of red and far-red light2017In: Plant, Cell and Environment, ISSN 0140-7791, E-ISSN 1365-3040, Vol. 40, no 8, p. 1332-1340Article in journal (Refereed)
    Abstract [en]

    We investigated the response to increasing intensity of red (R) and far-R (FR) light and to a decrease in R: FR ratio in Pinus sylvestris L. (Scots pine) seedling. The results showed that FR high-irradiance response for hypocotyl elongation may be present in Scots pine and that this response is enhanced by increasing light intensity. However, both hypocotyl inhibition and pigment accumulation were more strongly affected by the R light compared with FR light. This is in contrast to previous reports in Arabidopsis thaliana (L.) Heynh. In the angio-sperm, A. thaliana R light shows an overall milder effect on inhibition of hypocotyl elongation and on pigment biosynthesis compared with FR suggesting conifers and angiosperms respond very differently to the different light regimes. Scots pine shade avoidance syndrome with longer hypocotyls, shorter cotyledons and lower chlorophyll content in response to shade conditions resembles the response observed in A. thaliana. However, anthocyanin accumulation increased with shade in Scots pine, which again differs from what is known in angiosperms. Overall, the response of seedling development and physiology to R and FR light in Scots pine indicates that the regulatory mechanism for light response may differ between gymnosperms and angiosperms.

  • 27.
    Shaikhali, Jehad
    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).
    Barajas-Lopez, 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).
    Ötvös, Krisztina
    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).
    Garcia, Ana Sanchez
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Srivastava, Vaibhav
    Swedish Univ Agr Sci, Dept Forest Genet & Plant Physiol, Umea Plant Sci Ctr, S-90187 Umea, Sweden.
    Wingsle, Gunnar
    Swedish Univ Agr Sci, Dept Forest Genet & Plant Physiol, Umea Plant Sci Ctr, S-90187 Umea, Sweden.
    Bako, Laszlo
    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 CRYPTOCHROME1-Dependent Response to Excess Light Is Mediated through the Transcriptional Activators ZINC FINGER PROTEIN EXPRESSED IN INFLORESCENCE MERISTEM LIKE1 and ZML2 in Arabidopsis2012In: The Plant Cell, ISSN 1040-4651, E-ISSN 1532-298X, Vol. 24, no 7, p. 3009-3025Article in journal (Refereed)
    Abstract [en]

    Exposure of plants to light intensities that exceed the electron utilization capacity of the chloroplast has a dramatic impact on nuclear gene expression. The photoreceptor Cryptochrome 1 (cry1) is essential to the induction of genes encoding photoprotective components in Arabidopsis thaliana. Bioinformatic analysis of the cry1 regulon revealed the putative ciselement CryR1 (GnTCKAG), and here we demonstrate an interaction between CryR1 and the zinc finger GATA-type transcription factors ZINC FINGER PROTEIN EXPRESSED IN INFLORESCENCE MERISTEM LIKE1 (ZML1) and ZML2. The ZML proteins specifically bind to the CryR1 cis-element as demonstrated in vitro and in vivo, and TCTAG was shown to constitute the core sequence required for ZML2 binding. In addition, ZML2 activated transcription of the yellow fluorescent protein reporter gene driven by the CryR1 cis-element in Arabidopsis leaf protoplasts. T-DNA insertion lines for ZML2 and its homolog ZML1 demonstrated misregulation of several cry1-dependent genes in response to excess light. Furthermore, the zml1 and zml2 T-DNA insertion lines displayed a high irradiance-sensitive phenotype with significant photoinactivation of photosystem II (PSII), indicated by reduced maximum quantum efficiency of PSII, and severe photobleaching. Thus, we identified the ZML2 and ZML1 GATA transcription factors as two essential components of the cry1-mediated photoprotective response.

  • 28.
    Shaikhali, Jehad
    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, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Srivastava, Vaibhav
    Koenig, Janine
    Sauer, Uwe H.
    Umeå University, Faculty of Science and Technology, Department of Chemistry.
    Wingsle, Gunnar
    Dietz, Karl-Josef
    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).
    Redox-mediated Mechanisms Regulate DNA Binding Activity of the G-group of Basic Region Leucine Zipper (bZIP) Transcription Factors in Arabidopsis2012In: Journal of Biological Chemistry, ISSN 0021-9258, E-ISSN 1083-351X, Vol. 287, no 33, p. 27510-27525Article in journal (Refereed)
    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.

  • 29.
    Stachula, Paulina
    et al.
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology.
    Dios Barajas Lopez, Juan De
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology.
    Miskolczi, Pál
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology.
    Vaultier, Marie-Noelle
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology.
    Zheng, Bo
    Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC). Department of Forest Genetics and Plant Physiology, Swedish University of Agricultural Sciences.
    Ahad, Abdul
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology.
    Nick, Peter
    Molekulare Zellbiologie Botanisches Institut, Karlsruhe Institute of Technology, Germany.
    Bakó, László
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology.
    Strand, Åsa
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology.
    Hurry, Vaughan
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Department of Forest Genetics and Plant Physiology, Swedish University of Agricultural Sciences.
    CRMK1 a receptor-like kinase in the plasma membrane mediates the cold acclimation response in ArabidopsisManuscript (preprint) (Other academic)
  • 30.
    Strand, Åsa
    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).
    Foyer, C H
    Gustafsson, Petter
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Gardeström, Per
    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).
    Altering flux through the sucrose biosynthesis pathway in transgenic Arabidopsis thaliana modifies photosynthetic acclimation at low temperatures and the development of freezing tolerance2003In: Plant, Cell and Environment, ISSN 0140-7791, E-ISSN 1365-3040, Vol. 26, no 4, p. 523-535Article in journal (Refereed)
    Abstract [en]

    To test the hypothesis that the up-regulation of sucrose biosynthesis during cold acclimation is essential for the development of freezing tolerance, the acclimation responses of wild-type (WT) Arabidopsis thaliana (Heynh.) were compared with transgenic plants over-expressing sucrose phosphate synthase (over-sps) or with antisense repression of either cytosolic fructose-1,6-bisphosphatase (antifbp) or sucrose phosphate synthase (antisps). Plants were grown at 23 degreesC and then shifted to 5 degreesC. The leaves shifted to 5 degreesC for 10 d and the new leaves that developed at 5 degreesC were compared with control leaves on plants at 23 degreesC. Plants over-expressing sucrose phosphate synthase showed improved photosynthesis and increased flux of fixed carbon into sucrose when shifted to 5 degreesC, whereas both antisense lines showed reduced flux into soluble sugars relative to WT. The improved photosynthetic performance by the over-sps plants shifted to 5 degreesC was associated with an increase in freezing tolerance relative to WT (-9.1 and -7.2 degreesC, respectively). In contrast, both antisense lines showed impaired development of freezing tolerance (- 5.2 and -5.8 degreesC for antifbp and antisps, respectively) when shifted to 5 degreesC. In the new leaves developed at 5 degreesC the recovery of photosynthesis as typically seen in WT was strongly inhibited in both antisense lines and this inhibition was associated with a further failure of both antisense lines to cold acclimate. Thus, functional sucrose biosynthesis at low temperature in the over-sps plants reduced the inhibition of photosynthesis, maintained the mobilization of carbohydrates from source leaves to sinks and increased the rate at which freezing tolerance developed. Modification of sucrose metabolism therefore represents an additional approach that will have benefits both for the development of freezing tolerance and over-wintering, and for the supply of exportable carbohydrate to support growth at low temperatures.

  • 31.
    Strand, Åsa
    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).
    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).
    Gustafsson, Petter
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Gardeström, Per
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Development of Arabidopsis thaliana leaves at low temperatures releases the suppression of photosynthesis and photosynthetic gene expression despite the accumulation of soluble carbohydrates1997In: The Plant Journal, ISSN 0960-7412, E-ISSN 1365-313X, Vol. 12, no 3, p. 605-614Article in journal (Refereed)
    Abstract [en]

    Arabidopsis thaliana plants were grown at 23 degrees C end changes in carbohydrate metabolism, photosynthesis and photosynthetic gene expression were studied after the plants were shifted to 5 degrees C. The responses of leaves shifted to 5 degrees C after development at 23 degrees C are compared to leaves that developed at 5 degrees C. Shifting warm developed leaves to 5 degrees C lead to a severe suppression of photosynthesis that correlated with a rapid and sustained accumulation of hexose phosphates and soluble sugars. Associated with the suppression of photosynthesis and the accumulation of soluble sugars was a reduction in the amount of transcript for genes encoding photosynthetic proteins (cab and rbcS). In contrast, leaves that developed at 5 degrees C showed an increase in photosynthesis and control levels of photosynthetic gene expression. This recovery occurred even though leaves that developed at 5 degrees C maintained large pools of soluble sugars. Leaves that developed at 5 degrees C also showed a strong upregulation of the cytosolic pathway for soluble sugar synthesis but not of the chloroplastic pathway for starch synthesis. This was shown at the level of both enzyme activity and the amount of transcript. Thus, development of Arabidopsis leaves at 5 degrees C resulted in metabolic changes that enabled them to produce and accumulate large soluble sugar pools without any associated suppression of photosynthesis or photosynthetic gene expression. These changes were also associated with enhanced freezing tolerance. We suggest that this reprogramming of carbohydrate metabolism associated with development at tow temperature is essential to the development of full freezing tolerance and for winter survival of over-wintering herbaceous annuals.

  • 32.
    Strand, Åsa
    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).
    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).
    Henkes, S
    Huner, N
    Gustafsson, Petter
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Gardeström, Per
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Stitt, M
    Acclimation of Arabidopsis leaves developing at low temperatures. Increasing cytoplasmic volume accompanies increased activities of enzymes in the Calvin cycle and in the sucrose-biosynthesis pathway1999In: Plant Physiology, ISSN 0032-0889, E-ISSN 1532-2548, Vol. 119, no 4, p. 1387-1397Article in journal (Refereed)
    Abstract [en]

    Photosynthetic and metabolic acclimation to low growth temperatures were studied in Arabidopsis (Heynh.). Plants were grown at 23 degrees C and then shifted to 5 degrees C. We compared the leaves shifted to 5 degrees C for 10 d and the new leaves developed at 5 degrees C with the control leaves on plants that had been left at 23 degrees C. Leaf development at 5 degrees C resulted in the recovery of photosynthesis to rates comparable with those achieved by control leaves at 23 degrees C. There was a shift in the partitioning of carbon from starch and toward sucrose (Suc) in leaves that developed at 5 degrees C. The recovery of photosynthetic capacity and the redirection of carbon to Suc in these leaves were associated with coordinated increases in the activity of several Calvin-cycle enzymes, even larger increases in the activity of key enzymes for Suc biosynthesis, and an increase in the phosphate available for metabolism. Development of leaves at 5 degrees C also led to an increase in cytoplasmic volume and a decrease in vacuolar volume, which may provide an important mechanism for increasing the enzymes and metabolites in cold-acclimated leaves. Understanding the mechanisms underlying such structural changes during leaf development in the cold could result in novel approaches to increasing plant yield.

  • 33.
    Strand, Åsa
    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).
    Zrenner, R
    Trevanion, S
    Stitt, M
    Gustafsson, Petter
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Gardestrom, P
    Decreased expression of two key enzymes in the sucrose biosynthesis pathway, cytosolic fructose-1,6-bisphosphatase and sucrose phosphate synthase, has remarkably different consequences for photosynthetic carbon metabolism in transgenic Arabidopsis thaliana2000In: The Plant Journal, ISSN 0960-7412, E-ISSN 1365-313X, Vol. 23, no 6, p. 759-770Article in journal (Refereed)
    Abstract [en]

    Photosynthetic carbon metabolism was investigated in antisense Arabidopsis lines with decreased expression of sucrose phosphate synthase (SPS) and cytosolic fructose-1,6-bisphosphatase (cFBPase). In the light, triose phosphates are exported from the chloroplast and converted to sucrose via cFBPase and SPS. At night, starch is degraded to glucose, exported and converted to sucrose via SPS, cFBPase therefore lies upstream and SPS downstream of the point at which the pathways for sucrose synthesis in the day and night converge, Decreased cFBPase expression led to inhibition of sucrose synthesis; accumulation of phosphorylated intermediates; Pi-limitation of photosynthesis; and stimulation of starch synthesis. The starch was degraded to maintain higher levels of sugars and a higher rate of sucrose export during the night. This resembles the response in other species when expression of enzymes in the upper part of the sucrose biosynthesis pathway is reduced. Decreased expression of SPS inhibited sucrose synthesis, but phosphorylated intermediates did not accumulate and carbon partitioning was not redirected towards starch. Sugar levels and sucrose export was decreased during the night as well as during the day. Although ribulose-1,5-bisphosphate regeneration and photosynthesis were inhibited, the PGA/triose-P ratio remained low and the ATP/ADP ratio high, showing that photosynthesis was not limited by the rate at which Pi was recycled during end-product synthesis. Two novel responses counteracted the decrease in SPS expression and explain why phosphorylated intermediates did not accumulate, and why allocation was not altered in the antisense SPS lines. Firstly, a threefold decrease of PPI and a shift of the UDP-glucose/hexose phosphate ratio favoured sucrose synthesis and prevented the accumulation of phosphorylated intermediates. Secondly, there was no increase of AGPase activity relative to cFBPase activity, which would prevent a shift in carbon allocation towards starch synthesis. These responses are presumably triggered when sucrose synthesis is decreased in the night, as well as by day.

  • 34.
    Yang, Qi
    et al.
    Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC). Umeå University, Faculty of Science and Technology, Department of Plant Physiology. State Key Laboratory of Tree Genetics and Breeding, Chinese Academy of Forestry, Beijing, China.
    Blanco, Nicolás E.
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC). Centre of Photosynthetic and Biochemical Studies (CEFOBI-CONICET), Faculty of Biochemical Science and Pharmacy, Rosario National University, Rosario, Argentina.
    Hermida-Carrera, Carmen
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Lehotai, Nóra
    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
    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).
    Two dominant boreal conifers use contrasting mechanisms to reactivate photosynthesis in the spring2020In: Nature Communications, ISSN 2041-1723, E-ISSN 2041-1723, Vol. 11, no 1, article id 128Article in journal (Refereed)
    Abstract [en]

    Boreal forests are dominated by evergreen conifers that show strongly regulated seasonal photosynthetic activity. Understanding the mechanisms behind seasonal modulation of photosynthesis is crucial for predicting how these forests will respond to changes in seasonal patterns and how this will affect their role in the terrestrial carbon cycle. We demonstrate that the two co-occurring dominant boreal conifers, Scots pine (Pinus sylvestris L.) and Norway spruce (Picea abies), use contrasting mechanisms to reactivate photosynthesis in the spring. Scots pine downregulates its capacity for CO2 assimilation during winter and activates alternative electron sinks through accumulation of PGR5 and PGRL1 during early spring until the capacity for COassimilation is recovered. In contrast, Norway spruce lacks this ability to actively switch between different electron sinks over the year and as a consequence suffers severe photooxidative damage during the critical spring period.

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