The aim of our research is to dissect and elucidate the signalling pathways between the organelles and the nucleus that regulate the expression of nuclear genes encoding organellar proteins. We use an integrative approach with a combination of genetics, molecular biology, cell biology and biochemistry to understand the language of the chloroplasts and mitochondria.

Strand Asa 1150

The function of the eukaryotic cell depends on the regulated and reciprocal interaction between its different compartments. This includes not only the exchange of metabolic intermediates and energy equivalents, but also information. The presence of genes encoding organellar proteins in different cellular compartments necessitates a tight coordination of expression from the different genomes.The photosynthetic apparatus, for example, is composed of proteins encoded by genes from both the nucleus and the chloroplast and the expression of these genes is influenced by developmental and environmental cues. In the photosynthetic electron transport complexes of the thylakoid membrane, the core subunits are encoded by the plastidic genome and the peripheral subunits are encoded by the nuclear genome. In the stroma, the large subunit of RUBISCO is encoded by the plastid, whereas the small subunit is nuclear encoded. To ensure that all these photosynthetic complexes are assembled stoichiometrically, and to enable their rapid reorganization in response to a changing environment, the activities of the nuclear and chloroplast genomes must be closely coordinated through intracellular signalling.

asa_1 asa_2
Model of retrograde signalling between the chloroplast and the nucleus. The organelles produce multiple signals at different times of their development, and in response to changes in the environment, that orchestrate major changes in nuclear gene expression. We use Arabidopsis thaliana as a model to understand the role of retrograde communication during plant stress responses

asa_3TEMs of Arabidopsis mesophyll cells showing the chloroplast structuresThe necessity of a tight coordination of expression by the different genomes has led to the evolution of mechanisms to coordinate nuclear and organellar gene expression. These include both anterograde and retrograde controls. Anterograde mechanisms (nucleus-to-organelle) coordinate gene expression in the organelle, with cellular and environmental cues that are perceived and choreographed by proteins encoded in the nucleus. This type of traffic includes proteins that regulate the transcription and translation of organellar genes. Retrograde (organelle-to-nucleus) signalling, on the other hand, coordinates the expression of nuclear genes encoding organellar proteins with the metabolic and developmental state of the plastid and mitochondria through signals emitted from the organelles that regulate nuclear gene expression. The first evidence of retrograde signalling originated in plant sciences and the existence of a "plastid signal" came from studies of mutants with morphologically aberrant plastids. These mutants demonstrated reduced expression of nuclear-encoded plastid components suggesting that a plastid signal was emitted to repress the nuclear encoded photosynthesis genes. These results opened the research field to investigate how different plastid and mitochondrial processes trigger signals that modulate nuclear gene expression. We now know that several different plastid processes produce signals that regulate specific sets of genes or regulons and several molecular candidates for plastid signals have been described including tetrapyrroles, phosphonucleotides and ROS. Plastid signals play important and distinct roles both during the initial developmental stages (biogenic control) and in adult stage to face changing environmental conditions (operational control). Compared to plastid signals, less is known about the mitochondria retrograde regulation (MRR) in plants and in other systems. However, several studies indicate that, similar to the plastid signals, MRR is triggered by mitochondrial dysfunction such as disruption of the electron transport and accumulation of ROS. In my research group we are taking an integrative approach, using a combination of modern plant genetics, molecular biology, cell biology and biochemistry, to develop a comprehensive model describing the dynamic coordination of the different compartments in the eukaryotic cell and the importance of intracellular signalling for cellular energy homeostasis.
sweden_greySvensk sammanfattning

Publications list

  1. Establishment of Photosynthesis through Chloroplast Development Is Controlled by Two Distinct Regulatory Phases
    Plant Physiol. 2018 Feb;176(2):1199-1214
  2. Redox regulation of PEP activity during seedling establishment in Arabidopsis thaliana
    Nature Communications 2018, 9(1):50
  3. The role of retrograde signals during plant stress responses
    J Exp Bot. 2017, 69 (11):2783-2795
  4. Retrograde signals navigate the path to chloroplast development
    Plant Physiol. 2018, 176 (2):967-976
  5. A quantitative model of the phytochrome-PIF light signalling initiating chloroplast development
    SCIENTIFIC REPORTS 2017, 7 
  6. Establishment of photosynthesis is controlled by two distinct regulatory phases
    Plant Physiol. 2017 Jun 16 [Epub ahead of print]
  7. Differential response of Scots pine seedlings to variable intensity and ratio of R and FR ligh
    Plant, Cell & Environment,  2017, 40(8):1332-1340
  8. Circadian and Plastid Signaling Pathways Are Integrated to Ensure Correct Expression of the CBF and COR Genes during Photoperiodic Growth
    Plant Physiol. 2016, 171(2):1392-1406
  9. The Recovery of Plastid Function Is Required for Optimal Response to Low Temperatures in Arabidopsis
    PLoS One. 2015 Sep 14;10(9):e0138010
  10. Chloroplast transcription, untangling the Gordian Knot
    New Phytol. 2015 May;206(3):889-91
  11. Plastid encoded RNA polymerase activity and expression of photosynthesis genes required for embryo and seed development in Arabidopsis
    Front Plant Sci. 2014, 5:385
  12. Interaction between plastid and mitochondrial retrograde signalling pathways during changes to plastid redox status
    Philos Trans R Soc Lond B Biol Sci. 2014; 369(1640):20130231
  13. Barajas-López Jde D, Kremnev D, Shaikhali J, Piñas-Fernández A, Strand A
    PAPP5 Is Involved in the Tetrapyrrole Mediated Plastid Signalling during Chloroplast Development
    PLoS One. 2013; 8(3):e60305 Epub Mar 29.
  14. Cyclin-dependent kinase E1 (CDKE1) provides a cellular switch in plants between growth and stress responses
    J Biol Chem. 2013, 288(5):3449-59
  15. Shaikhali J, Barajas-Lopéz J, Ötvös K, Kremnev D, Sánchez Garcia A, Srivastava V, Wingsle G, Bako L, Strand Å
    The CRYPTOCHROME1-dependent response to excess light is mediated through the transcriptional activators ZINC FINGER PROTEIN EXPRESSED IN INFLORESCENCE MERISTEM LIKE1 and 2 in Arabidopsis
    Plant Cell, 2012, 24(7):3009-25
  16. Barajas-López J, Blanco NE, Strand A
    Plastid-to-nucleus communication, signals controlling the running of the plant cell
    BBA-Molecular Cell Research 2013, 1833(2):425-37
  17. Shaikhali J, Noren L, Barajas-Lopez JD, Srivastava V, Konig J, Sauer UH, Wingsle G, Dietz KJ, Strand A
    Redox-mediated mechanisms regulate DNA-binding activity of the G-group of bZIP transcription factors in Arabidopsis.
    J Biol Chem. 2012, 287(33):27510-25
  18. Kindgren P, Kremnev D, Blanco NE, de Dios Barajas López J, Fernández AP, Tellgren-Roth C, Small I, Strand A
    The plastid redox insensitive 2 mutant of Arabidopsis is impaired in PEP activity and high light-dependent plastid redox signalling to the nucleus
    Plant J. 2012, 70(2):279-91
  19. Kindgren P, Norén L, Barajas López JD, Shaikhali J, Strand A
    Interplay between HEAT SHOCK PROTEIN 90 and HY5 Controls PhANG Expression in Response to the GUN5 Plastid Signal
    Mol Plant. 2012 5(4):901-913
  20. Kindgren P, Eriksson MJ, Benedict C, Mohapatra A, Gough SP, Hansson M, Kieselbach T, Strand A
    A novel proteomic approach reveals a role for Mg-protoporphyrin IX in response to oxidative stress
    Physiologia Plantarum: 2011 141:310-320
  21. Piñas Fernández A, Strand Å
    Retrograde signalling and plant stress: plastid signals initiate cellular stress response
    Current Opinion in Plant Biology: 2008 11:509-513
  22. Fernandez AP, Strand A
    Signalling between the organelles and the nucleus
    Annual Plant Reviews (2008) 33:307–335
  23. Ankele E, Kindgren P, Pesquet E, Strand Å
    In Vivo visualization of Mg-ProtoporphyrinIX, a coordinator of photosynthetic gene expression in the nucleus and the chloroplast
    The Plant Cell: 2007 19:1964-1979
  24. Kleine T, Kindgren P, Benedict C, Hendrickson L, Strand Å
    Genome-wide gene expression analysis reveals a critical role for CRYPTOCHROME1 in response of Arabidopsis to high irradiance
    Plant Physiology: 2007 144:1391-1406
  25. Strand Å, Kleine T, Chory J
    The Structure and Function of Plastids. Plastid-to-nucleus signalling
    Advances in Photosynthesis and Respiration 2006, Chapter 9, 183-197
  26. Strand A
    Plastid-to-nucleus signalling
    Curr Opin Plant Biol: 2004 7:621-625
  27. Strand A, Foyer CH, Gustafsson P, Gardestrom P, Hurry V
    Altering flux through the sucrose biosynthesis pathway in transgenic Arabidopsis thaliana modifies photosynthetic acclimation at low temperatures and the development of freezing tolerance
    Plant Cell and Environment: 2003 26:523-535
  28. Strand A, Asami T, Alonso J, Ecker JR, Chory J
    Chloroplast to nucleus communication triggered by accumulation of Mg-protoporphyrinIX
    Nature: 2003 421:79-83
  29. Hurry V, Druart N, Cavaco A, Gardeström P, Strand A
    Photosynthesis at low temperatures: a case study with Arabidopsis
    In Plant Cold Hardiness: gene regulation and genetic engineering. (P.H. Li & E.T. Palva, eds). 2002, pp161-180
  30. Ganeteg U, Strand A, Gustafsson P, Jansson S
    The properties of the chlorophyll a/b-binding proteins Lhca2 and Lhca3 studied in vivo using antisense inhibition
    Plant Physiology: 2001 127:150-158
  31. Strand A, Zrenner R, Trevanion S, Stitt M, Gustafsson P, 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 thaliana
    Plant Journal: 2000 23:759-770
  32. Hurry V, Strand A, Furbank R, Stitt M
    The role of inorganic phosphate in the development of freezing tolerance and the acclimatization of photosynthesis to low temperature is revealed by the pho mutants of Arabidopsis thaliana
    Plant J: 2000 24:383-396
  33. Strand A, Hurry V, Henkes S, Huner N, Gustafsson P, Gardestrom P, 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 pathway
    Plant Physiology: 1999 119:1387-1397
  34. Strand A, Hurry V, Gustafsson P, Gardestrom P
    Development of Arabidopsis thaliana leaves at low temperatures releases the suppression of photosynthesis and photosynthetic gene expression despite the accumulation of soluble carbohydrates
    Plant Journal: 1997 12:605-614
  35. Hurry VM, Strand A, Tobiaeson M, Gardestrom P, Oquist G
    Cold Hardening of Spring and Winter-Wheat and Rape Results in Differential-Effects on Growth, Carbon Metabolism, and Carbohydrate Content
    Plant Physiology: 1995 109:697-706