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 (from "circa diem" which 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. 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.
In the daily context, we found that a functional clock and the 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 maintain cytokinin levels required for cell proliferation and growth, promoting biomass of plants.
Our very recent work places the photoreceptor and circadian clock protein ZTL (introduced above) as a critical integrator of light and circadian clock function with abscisic acid (ABA) signalling. ZTL promotes ABA-induced stomatal closure. It acts upstream of the PSEUDO-RESPONSE REGULATOR 5 (PRR5) to mitigate its function – but in addition ZTL also promotes ABA-induced gene expression and partner up with OPEN STOMATA 1 (OST1) to induce closing of stomata in response to ABA under drought stress. While timely expression of PRRs from dawn till dusk help keep stomata open, ZTL can short-cut and promote closure at the right time of day and in time of stress. Further, the role of ZTL is conserved between Arabidopsis and Populus trees. This picture (below) summarises our recent findings by Jurca et al., (2022).
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 its 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. We apply forward and reverse genetic 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.
Together, our studies of the circadian clock have contributed to understanding the importance of the circadian clock mechanism in weeds and trees: from its crucial impact on controlling water balance and photosynthesis through the control of stomatal regulation, to metabolism and synthesis of plant hormones as well as regulation of the cell cycle. Our future studies will further clarify the circadian clock mechanism and the important aspects of daily and seasonal timing for plant growth and development.
Key Publications
- Jurca, M., Sjölander, J., Ibáñez, C., Matrosova, A., Johansson, M., Kozarewa, I., Takata, N., Bakó, L., Webb, A. A. R., Israelsson-Nordström, M., & Eriksson, M. E. (2022) ZEITLUPE Promotes ABA-Induced Stomatal Closure in Arabidopsis and Populus. Frontiers in Plant Science https://doi.org/10.3389/fpls.2022.829121
- Edwards KD, Takata N, Johansson M, Jurca M, Novák O, Hényková E, Liverani S, Kozarewa I, Strnad M, Millar AJ, Ljung K, Eriksson ME (2018) Circadian clock components control daily growth activities by modulating cytokinin levels and cell division-associated gene expression in Populus trees. Plant Cell & Environment: 41(6):1468-1482 https://doi.org/10.1111/pce.13185
- Eriksson, M. E., Hoffman, D., Kaduk, M., Mauriat, M., & Moritz, T. (2015) 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, 205(3): 1288–1295. https://nph.onlinelibrary.wiley.com/doi/pdf/10.1111/nph.13144
- Johansson M, McWatters HG, Bakó L, Takata N, Gyula P, Hall A, Somers DE, Millar AJ, Eriksson ME (2011). Partners in time: EARLY BIRD associates with ZEITLUPE and regulates the speed of the Arabidopsis clock. Plant Physiology: 155:2108-2122 https://doi.org/10.1104/pp.110.167155
- Ashelford K, Eriksson ME, Allen CM, D’Amore L, Johansson M, Gould P, Kay S, Millar AJ, Hall N, Hall A (2011). Full genome re-sequencing reveals a novel circadian clock mutation in Arabidopsis. Genome Biology: 12:R28, 12 pp https://doi.org/10.1186/gb-2011-12-3-r28
- Ibáñez C, Kozarewa I, Johansson M, Ögren E, Rohde A, Eriksson ME (2010). Circadian clock components regulate entry and affect exit of seasonal dormancy as well as winter hardiness in Populus trees. Plant Physiology: 153:1823-1833 https://doi.org/10.1104/pp.110.158220
- Kozarewa I, Ibáñez C, Johansson M, Ögren E, Mozley D, Nylander E, Chono M, Moritz T, Eriksson ME (2010). Alteration of PHYA expression change circadian rhythms and timing of bud set in Populus. Plant Molecular Biology: 73:143-156 https://doi.org/10.1007/s11103-010-9619-2
- Eriksson ME, Hanano S, Southern MM, Hall A, Millar AJ (2003). Response regulator homologues have complementary, light- dependent functions in the Arabidopsis circadian clock. Planta: 218:159-162 https://doi.org/10.1007/s00425-003-1106-4
- Eriksson ME, Israelsson M, Olsson O, Moritz T (2000). Increased gibberellin biosynthesis in transgenic trees promotes growth, biomass production and xylem fiber length. Nature Biotechnology 18:784-788 https://doi.org/10.1038/77355
- Since 2016: Associate Professor, Dept. of Plant Physiology, Umeå University
- 2013: Docent, Dept. of Plant Physiology, Umeå University
- 2015-2016: Researcher, Dept. of Plant Physiology, Umeå University
- 2010-2014: Researcher, VINNMER Marie Curie International Qualification Fellow (VINNOVA, EU funded), Dept. of Plant Physiology, UPSC, Umeå University and Dept. of Plant Sciences Cambridge University, UK
- 2009-2010: Time limited lecturer 100 %, Dept. of Plant Physiology, Umeå University
- 2003-2008: Assistant professor (position externally funded by Formas), Dept. of Plant Physiology, Umeå University
- 2001-2003: Marie Curie Individual Research Fellow (position externally funded by EU), Dept. of Biological Sciences, Warwick University, UK
- 2000: PhD, Swedish University of Agricultural Sciences
- 1995, M.Sc. in Molecular Biology, Umeå University
- 1994: BSc, Uppsala University
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De flesta organismer har en biologisk klocka som gör att deras ämnesomsättning kan förutsäga förändringen mellan dag och natt. Då vi snabbt byter tidszoner får vi jet-lag eftersom vår inre biologiska klocka inte hinner med att ställa om till lokal tid lika fort som vi förflyttat oss.
Klockans funktion är att hjälpa djur och växter att i förväg anpassa sig till förändring i dagslängd och årstid, genom att den ställer om den inre tiden till återkommande förändringar i den yttre miljön, framförallt dagslängd och temperatur.
Jag använder backtrav och hybridasp med specifika genetiska förändringar som verktyg i studier av hur klockan är uppbyggd, hur den fungerar och vilken roll den spelar för hur växter anpassar tillväxt efter klimat och årstid.