Plants need highly efficient responses to adverse environmental conditions as they are bound to a single location. By totally their physiology plant can adapt to new environmental situations. These processes are in natural environments discriminative for plant fitness and in agricultural systems determining yield. Reprogrammed metabolism and changed translational patters are important elements of stress adaption. The goal of the group is to understand how plants adjust their metabolism and translation in response to a changing environment. On the longer term we want to use this knowledge to design better trees and crops.

Adverse environmental conditions often cause limited energy availability and plant cells respond to this by reprograming their metabolism to better fit the new situation. This dramatic change involves hundreds of gene products and metabolites; we call this the Low Energy Syndrome, LES. The change is mastered by the SnRK1 kinase complex, which is able to react to low levels of metabolizable sugars. This parallels the manner in which all eukaryotes regulate starvation responses. In plants the SnRK1 kinases regulate gene expression of genes encoding key metabolic enzymes by activating certain bZIP transcription factors. One of our projects focuses on these transcription factors. We are interested in their mode of action and how their activity is regulated. Technically we are using high throughput expression analysis (massive sequencing) and metabolic profiling as central analysis tools combined with genetics and transgene based methods.
Low energy availability and stress activate signaling cascades in the plant, initiated by activation of the SnRK1 kinase and resulting in changed metabolism and growth – The Low Energy Syndrome (LES). The aspects of interests for us are indicated.
When conditions are favorable for plant growth the SnRK1 complex is deactivated and a second major signaling system takes over mastered by another kinase - The Target of rapamycin, TOR that is positively regulates growth in all eukaryotes. TOR does so partly by regulating translation, which is a very energy consuming process and is therefore tightly regulated. The second major project in the laboratory deals with the regulatory mechanism of translational control by focusing on the activity of the ribosome. We currently are identifying novel components involved in translational changes using transcriptomics, translatomics, proteomics and genetic methodology.
The growing population of this planet will change our society. It is clear that food, feed and other plant-based resources will be limiting in the future. The grand challenge is to increase plant production a sustainable way. The transition to less fossil fuel dependent production will challenge our agricultural systems even further. Consequently, there is a basic need to optimize plant growth. This can be done by changed growth practices and reducing post-harvest losses, etc. However, we must use crop improvement to reach increased productivity similarly the green revolution half a decade ago. This is not limited to classical crops. We will need novel corps for biomass, bioenergy and biorefinery needs. By understanding the underlying mechanisms of growth-control we hope to find new ways to improve plant based production.
Translation is assayed using density gradients where polysomes (P, translating ribosomes) are separated from monosomes (M, non-translating ribosomes). Translation varies dramatically depending on experimental condition or developmental changes A) Translation is inhibited by 6h extended night and increased by sucrose treatments (6 h treatment of 100 mM sucrose), as indicated by increased relative levels of polysomes. Sucrose treatments compensate for the extended night treatment and allow continued translation although low energy input from the light. B) Ribosomal preparation from germinating seeds showing primarily monosomes in dry seeds (0h) and more translation (polysomes) during germination (5 to 72 hours) (Bai et al., 2017). C) In poplar buds, with primary monosomes present in the dormant winter buds and increased translation as the bud growth is initiated during the spring as evident from increased polysome levels (André and Mahboubi, unpublished). D) By Using RiboSeq we can map the translational activity of single ribosomes to mRNAs Image indicate the ribosomes bound to mRNA and after degrading the parts of the mRNA that is not bound by ribosome we can sequence the protected fragments. E) Resulting patterns of mapped reads (blue bars) representing fragments translated by active ribosomes on a mRNA sequence (red bars, thick parts representing Open reading frames). Distance between the ticks on the scale is 5 kbp
Key publications
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Hummel, M., Cordewener, J.H., de Groot, J.C., Smeekens, S.C.M., America, A.H., and Hanson, J. (2012). Dynamic protein composi- tion of Arabidopsis thaliana cytosolic ribosomes in response to sucrose feeding as revealed by label free MSE proteomics. Proteomics 12: 1024–1038.
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Ma, J., Hanssen, M., Lundgren, K., Hernandez, L., Delatte, T., Ehlert, A., Liu, C.M., Schluepmann, H., Droge-Laser, W., Moritz, T., Smeekens, S.C.M., and Hanson, J. (2011). The sucrose-regulated Arabidopsis transcription factor bZIP11 reprograms metabolism and regulates trehalose metabolism. New Phytol 191: 733–745.
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Rahmani, F., Hummel, M., Schuurmans, J.A., Wiese-Klinkenberg, A., Smeekens, S.C.M., and Hanson, J. (2009). Sucrose control of translation mediated by an upstream open reading frame-encoded peptide. Plant Physiol 150: 1356–1367.
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Smeekens, S.C.M., Ma, J., Hanson, J., and Rolland, F. (2010). Sugar signals and molecular networks controlling plant growth. Current opinion in plant biology 13: 274–279.
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Hanson, J. and Smeekens, S.C.M. (2009). Sugar perception and signaling--an update. Current opinion in plant biology 12: 562–567.
CV Dr. Johannes Hanson
- 1993 MSc Uppsala University
- 2000 PhD Uppsala University
- 2000-03 Post doc and lecturer Uppsala University
- 2003-08 Post doc Utrecht University,
- 2008 Assistant professor, Utrecht University
- 2011 Associate professor, UPSC, Umeå University
Publication list
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Arabidopsis bZIP11 is a susceptibility factor during Pseudomonas syringae infection
Mol Plant Microbe Interact. 2021 Jan 5 Epub ahead of print
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Metabolite Control of Translation by Conserved Peptide uORFs: The Ribosome as a Metabolite Multisensor
Plant Physiol 2020, 182(1):110-122
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Seed stored mRNAs that are specifically associated to monosome-are translationally regulated during germination
Plant Physiol. 2020:182(1):378-392
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Defence priming in Arabidopsis and Seeds – a Meta-Analysis
Scientific Reports 2019, 9(1):13309
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Metabolite Control of Translation by Conserved Peptide uORFs: The Ribosome as a Metabolite Multi-sensor
Plant Physiol. 2019 Aug 26 [Epub ahead of print]
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Novel pipeline identifies new upstream ORFs and non-AUG initiating main ORFs with conserved amino acid sequences in the 5' leader of mRNAs in Arabidopsis thaliana
RNA. 2018: 25(3):292-304
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Establishment of Photosynthesis through Chloroplast Development Is Controlled by Two Distinct Regulatory Phases
Plant Physiol. 2018 Feb;176(2):1199-1214
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Combined transcriptome and translatome analyses reveal a role for tryptophan-dependent auxin biosynthesis in the control of DOG1-dependent seed dormancy
New Phytol. 2018, 217 (3):1077-1085
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Differentially expressed genes during the imbibition of dormant and after-ripened seeds - a reverse genetics approach
BMC Plant Biol. 2017, 17(1):151
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Establishment of photosynthesis is controlled by two distinct regulatory phases
Plant Physiol. 2017 Jun 16 [Epub ahead of print]
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The Arabidopsis bZIP11 transcription factor links low-energy signalling to auxin-mediated control of primary root growth
PLoS Genet. 2017 Feb 3;13(2):e1006607
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Shaping plant development through the SnRK1-TOR metabolic regulators
Curr Opin Plant Biol. 2016, 35:152-157
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Extensive translational regulation during seed germination revealed by polysomal profiling
New Phytol. 2017, 214(1):233-244
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The Arabidopsis TOR Kinase Specifically Regulates the Expression of Nuclear Genes Coding for Plastidic Ribosomal Proteins and the Phosphorylation of the Cytosolic Ribosomal Protein S6
Front Plant Sci. 2016, 7:1611
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Quantitative phosphoproteomics reveals the role of the AMPK plant ortholog SnRK1 as a metabolic master regulator under energy deprivation
Sci Rep. 2016, 6:31697
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The phylogeny of C/S1 bZIP transcription factors reveals a shared algal ancestry and the pre-angiosperm translational regulation of S1 transcripts
Sci Rep. 2016 Jul 26;6:30444
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TOR Signaling and Nutrient Sensing
Annu Rev Plant Biol. 2016, 67:261-285
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The Arabidopsis DELAY OF GERMINATION 1 gene affects ABSCISIC ACID INSENSITIVE 5 (ABI5) expression and genetically interacts with ABI3 during Arabidopsis seed development
Plant J. 2016, 85(4):451-465
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Effects of Parental Temperature and Nitrate on Seed Performance are Reflected by Partly Overlapping Genetic and Metabolic Pathways.
Plant Cell Physiol. 2016, 57(3):473-487
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SnRK1-triggered switch of bZIP63 dimerization mediates the low-energy response in plants
Elife. 2015;4:e05828
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Rhizobacterial volatiles and photosynthesis-related signals coordinate MYB72 in Arabidopsis roots during onset of induced systemic resistance and iron deficiency responses
Plant J. 2015, 84(2):309-322
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Crosstalk between Two bZIP Signaling Pathways Orchestrates Salt-Induced Metabolic Reprogramming in Arabidopsis Roots
Plant Cell. 2015, 27(8):2244-2260
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Proteomic LC-MS analysis of Arabidopsis cytosolic ribosomes: Identification of ribosomal protein paralogs and re-annotation of the ribosomal protein genes
J Proteomics. 2015, 128 436-449
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Increased sucrose levels mediate selective mRNA translation in Arabidopsis
BMC Plant Biol. 2014, 14(1):306
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β-Glucosidase BGLU42 is a MYB72-dependent key regulator of rhizobacteria-induced systemic resistance and modulates iron deficiency responses in Arabidopsis roots
New Phytol. 2014; 204(2):368-79
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Sugar signals and the control of plant growth and development
J Exp Bot. 2014; 65(3):799-807
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ABI4: versatile activator and repressor
Trends Plant Sci. 2012 Nov 19. [Epub ahead of print]
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Hummel M, Cordewener JH, de Groot JC, Smeekens S, America AH, Hanson J
Dynamic protein composition of Arabidopsis thaliana cytosolic ribosomes in response to sucrose feeding as revealed by label free MS(E) proteomics
Proteomics 2012 12(7):1024-38
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Ma J, Hanssen M, Lundgren K, Hernández L, Delatte T, Ehlert A, Liu C-M, Schluepmann H, Dröge-Laser W, Moritz T, Smeekens S, Hanson J
The sucrose-regulated Arabidopsis transcription factor bZIP11 reprograms metabolism and regulates trehalose metabolism
New Phytologist: 2011, 191:733–745
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Li P, Wind JJ, Shi X, Zhang H, Hanson J, Smeekens SC, Teng S
Fructose sensitivity is suppressed in Arabidopsis by the transcription factor ANAC089 lacking the membrane-bound domain
Proceedings of the National Academy of Sciences of the United States of America: 2011 108:3436-3441
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Sucrose: metabolite and signaling molecule
Phytochemistry: 2010 71:1610-1614
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Sugar signals and molecular networks controlling plant growth
Current Opinion in Plant Biology: 2010 13:274-279
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Natural variation for seed dormancy in Arabidopsis is regulated by additive genetic and molecular pathways
Proceedings of the National Academy of Science of the United States of America: 2010 107:4264-4269
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Hanson J, Smeekens S
Sugar perception and signaling--an update
Current Opinion in Plant Biology: 2009 12:562-567
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Hummel M, Rahmani F, Smeekens S, Hanson J
Sucrose mediated translational control
Annals of Botany: 2009 104:1-7
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Rahmani F, Hummel M, Schuurmans J, Wiese-Klinkenberg A, Smeekens S, Hanson J
Sucrose control of translation mediated by a uORF encoded peptide
Plant Physiology: 2009 150:1356-1367
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Weltmeier F, Rahmani F, Ehlert A, Dietrich K, Schütze K, Wang X, Chaban C, Hanson J, Teige M, Harter K, Vicente-Carbajosa J, Smeekens S, Dröge-Laser W
Expression patterns within the Arabidopsis C/S1 bZIP transcription factor network: availability of heterodimerization partners controls gene expression during stress response and development
Plant Molecular Biology: 2009 69:107-19
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Hanson J, Hanssen M, Wiese A, Hendriks MM, Smeekens S
The sucrose regulated transcription factor bZIP11 affects amino acid metabolism by regulating the expression of ASPARAGINE SYNTHETASE1 and PROLINE DEHYDROGENASE2
Plant Journal: 2008 53:935-49.
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Henriksson E, Olsson AS, Johannesson H, Johansson H, Hanson J, Engström P, Söderman E
Homeodomain leucine zipper class I genes in Arabidopsis. Expression patterns and phylogenetic relationships
Plant Physiology: 2005 139:509-518
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Johannesson H, Wang Y, Hanson J, Engström P
The Arabidopsis thaliana homeobox gene ATHB5 is a potential regulator of abscisic acid responsiveness in developing seedlings
Plant Molecular Biology: 2003 51:719-29
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Hanson J, Regan S, Engström P
The expression pattern of the homeobox gene ATHB13 reveals a conservation of transcriptional regulatory mechanisms between Arabidopsis and hybrid aspen
Plant Cell Reports: 2002 21:80-89
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Hanson J, Johannesson H, Engström P
Sugar-dependent alterations in cotyledon and leaf development in transgenic plants expressing the HDZip gene ATHB13
Plant Molecular Biology: 2001 45:247-62