The focus of the research group is to understand the functional aspects of the circadian clockwork in Arabidopsis and trees (Populus and other species), and how this timing machinery regulates growth. To anticipate the diurnal cycle of light and dark during a day and to anticipate the seasonal changes, most organisms have developed a molecular time measuring system called a circadian ("circadian" in Latin means "about a day") oscillator or clock. Light and temperature can be received by multiple photoreceptors in the red, far-red and blue spectra and mediates re-setting of this clock.

Photo of Maria Eriksson; Title: Timing is everything, also for weeds and trees.Timing is everything, also for weeds and trees.

In Arabidopsis, there are five red/far-red light photoreceptors called phytochromes (phy). The best characterized are phyA (far-red) and phyB (red). In the blue wavelengths, receptors like the cryptochromes (cry1 and cry2) are important, but also the ZEITLUPE (ZTL) gene family of F-box, Kelch-, and LOV/PAS domain containing proteins are capable of receiving blue light directly to regulate the circadian clock and seasonal timing. A central loop includes the morning expressed CIRCADIAN CLOCK ASSOCIATED1 (CCA1), and LATE ELONGATED HYPOCOTYL (LHY) which are MYB transcription factors that negatively regulate the gene expression of TIMING OF CAB2 EXPRESSION 1 (TOC1) so that it is expressed in the evening when CCA1 and LHY are turned over. TOC1 in turn mitigate expression of CCA1 and LHY. In addition, this negative feedback loop is intertwined with at least two additional interlocked feedback loops.

Populus orthologues of core clock genes LATE ELONGATED 1 (LHY1), LHY2 and TOC1 were targeted by RNA interference (RNAi) and allowed us to experimentally test their clock function and effect on growth. These studies showed that the circadian clock of Populus sp. trees contain a negative feedback loop of LHY1, LHY2 with TOC1 – similar to the situation in Arabidopsis. Our Populus ‘clock mutant’ RNAi trees also helped us to show that these proteins control seasonal timing of growth, cold response and freezing tolerance of trees.

 Signs of season. An apex of Populus in active growth (upper left), at bud set (upper right), during dormancy (lower right) and at bud burst (lower left). Signs of season. An apex of Populus in active growth (upper left), at bud set (upper right), during dormancy (lower right) and at bud burst (lower left)

Also, in the daily context, we found that a functional clock and importantly expression of the morning clock genes LHY1 and LHY2 are needed for growth. A key aspect of their regulation is obtained through regulation of CYCLIN D3 expression and thereby the G1 to S-phase transition of the cell cycle. Their functions are also needed to support cytokinin levels required for cell proliferation and growth, promoting biomass of plants. Hence, as we learn more about temporal regulation, there is a great potential for biotechnological application in adapting new plants or re-adapting (in case of climate warming) local plants to rapidly evolving "new" local conditions. Such adaptation may involve a means to increase the length of critical daylength requirements of plants to match a novel growth season, while keeping winter hardiness, as well as increasing biomass production.

To experimentally explore clock function and tits role in growth, we use Arabidopsis thaliana for gene discovery. As tree model systems, we mainly use the deciduous tree hybrid aspen (Populus tremula x P. tremuloides) and the gymnosperm Norway spruce (Picea abies) to address the clock’s role in wood regulation and growth. By using forward and reverse genetics approaches as well as assays of natural variation, as appropriate.

In the laboratory, we also use a combination of bioinformatics, genetic and molecular tools with in vitro/in vivo studies to study clock and protein function. Such tools for studying the clockwork and its adaptive value include plant cells or plants with altered levels of clock gene expression, molecular tools such as RNAseq, promoter:LUCIFERASE expression, real time PCR and protein assays to monitor circadian clock regulated gene and protein expression. To investigate perennial growth, we monitor elongation and diameter growth as well as physiological manifestations of season such as flowering, growth cessation, bud set and bud break. Mutants with an altered timing mechanism in this way help us to build a model for clock function and its impact on daily and seasonal regulation of growth.

Populus trees carrying firefly LUCIFERASE under control of a circadianly controlled promoterPopulus trees carrying firefly LUCIFERASE under control of a circadianly controlled promoter

Together, our studies of the circadian clock offer a possibility to further the understanding of the timing mechanism in the life of a plant, its impact on metabolism and the synthesis of plant hormones as well as regulation of the cell cycle - all deciding plant growth.


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Publication list

  1. Growing in time: Exploring the molecular mechanisms of tree growth
    Tree Physiol. 2020 May 29 [Epub ahead of print]
  2. GIGANTEA-like genes control seasonal growth cessation in Populus
    New Phytol. 2018, 218 (4):1491-1503
  3. Circadian clock components control daily growth activities by modulating cytokinin levels and cell division-associated gene expression in Populus trees
    Plant Cell Environ. 2018, 41 (6):1468-1482
  4. Autumn senescence in aspen is not triggered by day length
    Physiol Plant. 2018, 162(1):123-134
  5. 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
  6. Plant Circadian Rhythms -based in part on the version published 2007
    eLS, 1-10 2016
  7. Role of the circadian clock in cold acclimation and winter dormancy in perennial plants
    In "Advances in dormancy", 2015, Ed Anderson J, Springer New York
  8. Transgenic hybrid aspen trees with increased gibberellin (GA) concentrations suggest that GA acts in parallel with FLOWERING LOCUS T2 to control shoot elongation
    New Phytologist 2015, 205(3):1288-95
  9. The perennial clock is an essential timer for seasonal growth events and cold hardiness
    Plant Circadian Networks, 297-311 2014
  10. Monitoring seasonal bud set, bud burst, and cold hardiness in Populus
    Plant Circadian Networks, 313-324 1 2014
  11. Takata N, Eriksson ME
    A simple and efficient transient transformation for hybrid aspen (Populus tremula × P. tremuloides)
    Plant Methods 2012, 8:30
  12. Cooke JE, Eriksson ME, Junttila O
    The Dynamic Nature of Bud Dormancy in Trees: Environmental Control and Molecular Mechanisms
    Plant Cell Environ. 2012 10(35):1707-1728
  13. Plant cell responses to cold are all about timing
    Curr Opin Plant Biol. 2011 Dec;14(6):731-7
  14. Ashelford K, Eriksson ME, Allen CM, D'Amore L, Johansson M, Gould P, Kay S, Millar AJ, Hall N, Hall A
    Full genome re-sequencing reveals a novel circadian clock mutation in Arabidopsis
    Genome Biology: 2011 12:R28, 12 pp
  15. Johansson M, McWatters HG, Bakó L, Takata N, Gyula P, Hall A, Somers DE, Millar AJ, Eriksson ME
    Partners in time: EARLY BIRD associates with ZEITLUPE and regulates the speed of the Arabidopsis clock
    Plant Physiology: 2011 155:2108-2122
  16. Ibáñez C, Kozarewa I, Johansson M, Ögren E, Rohde A, Eriksson ME
    Circadian clock components regulate entry and affect exit of seasonal dormancy as well as winter hardiness in Populus trees
    Plant Physiology: 2010 153:1823-1833
  17. Kozarewa I, Ibáñez C, Johansson M, Ögren E, Mozley D, Nylander E, Chono M, Moritz T, Eriksson ME
    Alteration of PHYA expression change circadian rhythms and timing of bud set in Populus
    Plant Molecular Biology: 2010 73:143-156
  18. Hoffman DE, Jonsson P, Bylesjö M, Trygg J, Antti H, Eriksson ME, Moritz T
    Changes in diurnal patterns within the Populus transcriptome and metabolome in response to photoperiod variation
    Plant, Cell & Environment: 2010 33:1298-1313
  19. Plant Circadian Rhythms
    eLS 2007
  20. Kevei E, Gyula P, Hall A, Kozma-Bognar L, Kim WY, Eriksson ME, Toth R, Hanano S, Feher B, Southern MM, Bastow RM, Viczian A, Hibberd V, Davis SJ, Somers DE, Nagy F, Millar AJ
    Forward genetic analysis of the circadian clock separates the multiple functions of ZEITLUPE
    Plant Physiology: 2006 140:933-945
  21. Israelsson M, Eriksson ME, Hertzberg M, Aspeborg H, Nilsson P, Moritz T
    Changes in gene expression in the wood-forming tissue of transgenic hybrid aspen with increased secondary growth
    Plant Mol Biol: 2003 52:893-903
  22. Eriksson ME, Millar AJ
    The circadian clock. A plant's best friend in a spinning world
    Plant Physiol: 2003 132:732-738
  23. Eriksson ME, Hanano S, Southern MM, Hall A, Millar AJ
    Response regulator homologues have complementary, light-dependent functions in the Arabidopsis circadian clock
    Planta: 2003 218:159-162
  24. Eriksson ME, Moritz T
    Daylength and spatial expression of a gibberellin 20-oxidase isolated from hybrid aspen (Populus tremula L. x P. tremuloides Michx.)
    Planta: 2002 214:920-930
  25. Eriksson ME, Israelsson M, Olsson O, Moritz T
    Increased gibberellin biosynthesis in transgenic trees promotes growth, biomass production and xylem fiber length
    Nature Biotechnology 2000 18:784-788
  26. Olsen JE, Junttila O, Nilsen J, Eriksson ME, Martinussen I, Olsson O, Sandberg G, Moritz T
    Ectopic expression of oat phytochrome A in hybrid aspen changes critical daylength for growth and prevents cold acclimatization
    Plant Journal: 1997 12:1339-1350
  27. Eriksson ME, Moritz T
    Isolation of a cDNA Encoding a Phytochrome A (Accession No.AJ001318) from Populus tremula x tremuloides. (PGR97-186)
    Plant Physiology: 1997 115:1731-1731