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  • 1. Baena-González, Elena
    et al.
    Hanson, Johannes
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology.
    Shaping plant development through the SnRK1–TOR metabolic regulators2017In: Current opinion in plant biology, ISSN 1369-5266, E-ISSN 1879-0356, Vol. 35, p. 152-157Article in journal (Refereed)
    Abstract [en]

    SnRK1 (Snf1-related protein kinase 1) and TOR (target of rapamycin) are evolutionarily conserved protein kinases that lie at the heart of energy sensing, playing central and antagonistic roles in the regulation of metabolism and gene expression. Increasing evidence links these metabolic regulators to numerous aspects of plant development, from germination to flowering and senescence. This prompts the hypothesis that SnRK1 and TOR modify developmental programs according to the metabolic status to adjust plant growth to a specific environment. The aim of this review is to provide support to this hypothesis and to incentivize further studies on this topic by summarizing the work that establishes a genetic connection between SnRK1-TOR and plant development.

  • 2. Bai, Bing
    et al.
    Novák, Ondrej
    Ljung, Karin
    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. Molecular Plant Physiology, Institute of Environmental Biology, Utrecht University, 3584 CH Utrecht, the Netherlands.
    Bentsink, Leonie
    Combined transcriptome and translatome analyses reveal a role for tryptophan-dependent auxin biosynthesis in the control of DOG1-dependent seed dormancy2018In: New Phytologist, ISSN 0028-646X, E-ISSN 1469-8137, Vol. 217, no 3, p. 1077-1085Article in journal (Refereed)
    Abstract [en]

    The importance of translational regulation during Arabidopsis seed germination has been shown previously. Here the role of transcriptional and translational regulation during seed imbibition of the very dormant DELAY OF GERMINATION 1 (DOG1) near-isogenic line was investigated. Polysome profiling was performed on dormant and after-ripened seeds imbibed for 6 and 24 h in water and in the transcription inhibitor cordycepin. Transcriptome and translatome changes were investigated. Ribosomal profiles of after-ripened seeds imbibed in cordycepin mimic those of dormant seeds. The polysome occupancy of mRNA species is not affected by germination inhibition, either as a result of seed dormancy or as a result of cordycepin treatment, indicating the importance of the regulation of transcript abundance. The expression of auxin metabolism genes is discriminative during the imbibition of after-ripened and dormant seeds, which is confirmed by altered concentrations of indole-3-acetic acid conjugates and precursors.

  • 3.
    Bai, Bing
    et al.
    Department of Molecular Plant Physiology, Utrecht University, 3584 CH Utrecht, the Netherlands; Wageningen Seed Laboratory, Laboratory of Plant Physiology, Wageningen University, 6708 PB Wageningen, the Netherlands.
    Peviani, Alessia
    van der Horst, Sjors
    Gamm, Magdalena
    Snel, Berend
    Bentsink, Leónie
    Hanson, Johannes
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Department of Molecular Plant Physiology, Utrecht University, 3584 CH Utrecht, the Netherlands.
    Extensive translational regulation during seed germination revealed by polysomal profiling2017In: New Phytologist, ISSN 0028-646X, E-ISSN 1469-8137, Vol. 214, no 1, p. 233-244Article in journal (Refereed)
    Abstract [en]

    This work investigates the extent of translational regulation during seed germination. The polysome occupancy of each gene is determined by genome-wide profiling of total mRNA and polysome-associated mRNA. This reveals extensive translational regulation during Arabidopsis thaliana seed germination. The polysome occupancy of thousands of individual mRNAs changes to a large extent during the germination process. Intriguingly, these changes are restricted to two temporal phases (shifts) during germination, seed hydration and germination. Sequence features, such as upstream open reading frame number, transcript length, mRNA stability, secondary structures, and the presence and location of specific motifs correlated with this translational regulation. These features differed significantly between the two shifts, indicating that independent mechanisms regulate translation during seed germination. This study reveals substantial translational dynamics during seed germination and identifies development-dependent sequence features and cis elements that correlate with the translation control, uncovering a novel and important layer of gene regulation during seed germination.

  • 4.
    Bentsink, Leónie
    et al.
    aDepartment of Molecular Plant Physiology, Utrecht University, Utrecht, The Netherlands; Laboratory of Genetics, Wageningen University, Wageningen, The Netherlands.
    Hanson, Johannes
    Molecular Plant Physiology, Utrecht University, Utrecht, The Netherlands; Centre for BioSystems Genomics, Wageningen, The Netherlands.
    Hanhart, Corrie J
    Wageningen, The Netherlands.
    Blankestijn-de Vries, Hetty
    Wageningen, The Netherlands.
    Coltrane, Colin
    Wageningen, The Netherlands.
    Keizer, Paul
    Wageningen, The Netherlands.
    El-Lithy, Mohamed
    Wageningen, The Netherlands.
    Alonso-Blanco, Carlos
    Madrid, Spain.
    de Andrés, M Teresa
    Madrid, Spain.
    Reymond, Matthieu
    Cologne, Germany.
    van Eeuwijk, Fred
    Wageningen, The Netherlands.
    Smeekens, Sjef
    Molecular Plant Physiology, Utrecht University, Utrecht, The Netherlands; Centre for BioSystems Genomics, Wageningen, The Netherlands.
    Koornneef, Maarten
    Wageningen, The Netherlands; Cologne, Germany.
    Natural variation for seed dormancy in Arabidopsis is regulated by additive genetic and molecular pathways2010In: Proceedings of the National Academy of Sciences of the United States of America, ISSN 0027-8424, E-ISSN 1091-6490, Vol. 107, no 9, p. 4264-4269Article in journal (Refereed)
    Abstract [en]

    Timing of germination is presumably under strong natural selection as it determines the environmental conditions in which a plant germinates and initiates its postembryonic life cycle. To investigate how seed dormancy is controlled, quantitative trait loci (QTL) analyses has been performed in six Arabidopsis thaliana recombinant inbred line populations by analyzing them simultaneously using a mixed model QTL approach. The recombinant inbred line populations were derived from crosses between the reference accession Landsberg erecta (Ler) and accessions from different world regions. In total, 11 delay of germination (DOG) QTL have been identified, and nine of them have been confirmed by near isogenic lines (NILs). The absence of strong epistatic interactions between the different DOG loci suggests that they affect dormancy mainly by distinct genetic pathways. This was confirmed by analyzing the transcriptome of freshly harvested dry seeds of five different DOG NILs. All five DOG NILs showed discernible and different expression patterns compared with the expression of their genetic background Ler. The genes identified in the different DOG NILs represent largely different gene ontology profiles. It is proposed that natural variation for seed dormancy in Arabidopsis is mainly controlled by different additive genetic and molecular pathways rather than epistatic interactions, indicating the involvement of several independent pathways.

  • 5. Dekkers, Bas J W
    et al.
    He, Hanzi
    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. Department of Molecular Plant Physiology, Utrecht University, CH, Utrecht, The Netherlands.
    Willems, Leo A J
    Jamar, Diaan C L
    Cueff, Gwendal
    Rajjou, Loïc
    Hilhorst, Henk W M
    Bentsink, Leónie
    The Arabidopsis DELAY OF GERMINATION 1 gene affects ABSCISIC ACID INSENSITIVE 5 (ABI5) expression and genetically interacts with ABI3 during Arabidopsis seed development2016In: The Plant Journal, ISSN 0960-7412, E-ISSN 1365-313X, Vol. 85, no 4, p. 451-465Article in journal (Refereed)
    Abstract [en]

    The seed expressed gene DELAY OF GERMINATION (DOG) 1 is absolutely required for the induction of dormancy. Next to a non-dormant phenotype, the dog1-1 mutant is also characterized by a reduced seed longevity suggesting that DOG1 may affect additional seed processes as well. This aspect however, has been hardly studied and is poorly understood. To uncover additional roles of DOG1 in seeds we performed a detailed analysis of the dog1 mutant using both transcriptomics and metabolomics to investigate the molecular consequences of a dysfunctional DOG1 gene. Further, we used a genetic approach taking advantage of the weak aba insensitive (abi) 3-1 allele as a sensitized genetic background in a cross with dog1-1. DOG1 affects the expression of hundreds of genes including LATE EMBRYOGENESIS ABUNDANT and HEAT SHOCK PROTEIN genes which are affected by DOG1 partly via control of ABI5 expression. Furthermore, the content of a subset of primary metabolites, which normally accumulate during seed maturation, was found to be affected in the dog1-1 mutant. Surprisingly, the abi3-1 dog1-1 double mutant produced green seeds which are highly ABA insensitive, phenocopying severe abi3 mutants, indicating that dog1-1 acts as an enhancer of the weak abi3-1 allele and thus revealing a genetic interaction between both genes. Analysis of the dog1 and dog1 abi3 mutants revealed additional seed phenotypes and therefore we hypothesize that DOG1 function is not limited to dormancy but that it is required for multiple aspects of seed maturation, in part by interfering with ABA signalling components.

  • 6.
    Dobrenel, Thomas
    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. Institut Jean-Pierre Bourgin, UMR 1318 INRA AgroParisTech, ERL CNRS 3559, Saclay Plant Sciences, Versailles 78026, France.
    Caldana, Camila
    Hanson, Johannes
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Robaglia, Christophe
    Vincentz, Michel
    Veit, Bruce
    Meyer, Christian
    TOR Signaling and Nutrient Sensing2016In: Annual Review of Plant Biology, ISSN 1543-5008, E-ISSN 1545-2123, Vol. 67, p. 261-285Article, review/survey (Refereed)
    Abstract [en]

    All living organisms rely on nutrients to sustain cell metabolism and energy production, which in turn need to be adjusted based on available resources. The evolutionarily conserved target of rapamycin (TOR) protein kinase is a central regulatory hub that connects environmental information about the quantity and quality of nutrients to developmental and metabolic processes in order to maintain cellular homeostasis. TOR is activated by both nitrogen and carbon metabolites and promotes energy-consuming processes such as cell division, mRNA translation, and anabolism in times of abundance while repressing nutrient remobilization through autophagy. In animals and yeasts, TOR acts antagonistically to the starvation-induced AMP-activated kinase (AMPK)/sucrose nonfermenting 1 (Snf1) kinase, called Snf1-related kinase 1 (SnRK1) in plants. This review summarizes the immense knowledge on the relationship betweenTORsignaling and nutrients in nonphotosynthetic organisms and presents recent findings in plants that illuminate the crucial role of this pathway in conveying nutrient-derived signals and regulating many aspects of metabolism and growth.

  • 7.
    Dobrenel, Thomas
    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. Institut Jean-Pierre Bourgin, Institut National de la Recherche Agronomique, AgroParisTech, Centre National de la Recherche Scientifique, Université Paris-Saclay, Versailles, France; Université Paris-Sud–Université Paris-Saclay, Orsay, France.
    Mancera-Martinez, Eder
    Forzani, Celine
    Azzopardi, Marianne
    Davanture, Marlene
    Moreau, Manon
    Schepetilnikov, Mikhail
    Chicher, Johana
    Langella, Olivier
    Zivy, Michel
    Robaglia, Christophe
    Ryabova, Lyubov A.
    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.
    Meyer, Christian
    The Arabidopsis TOR Kinase Specifically Regulates the Expression of Nuclear Genes Coding for Plastidic Ribosomal Proteins and the Phosphorylation of the Cytosolic Ribosomal Protein S62016In: Frontiers in Plant Science, ISSN 1664-462X, E-ISSN 1664-462X, Vol. 7, article id 1611Article in journal (Refereed)
    Abstract [en]

    Protein translation is an energy consuming process that has to be fine-tuned at both the cell and organism levels to match the availability of resources. The target of rapamycin kinase (TOR) is a key regulator of a large range of biological processes in response to environmental cues. In this study, we have investigated the effects of TOR inactivation on the expression and regulation of Arabidopsis ribosomal proteins at different levels of analysis, namely from transcriptomic to phosphoproteomic. TOR inactivation resulted in a coordinated down-regulation of the transcription and translation of nuclear-encoded mRNAs coding for plastidic ribosomal proteins, which could explain the chlorotic phenotype of the TOR silenced plants. We have identified in the 5' untranslated regions (UTRs) of this set of genes a conserved sequence related to the 5' terminal oligopyrimidine motif, which is known to confer translational regulation by the TOR kinase in other eukaryotes. Furthermore, the phosphoproteomic analysis of the ribosomal fraction following TOR inactivation revealed a lower phosphorylation of the conserved Ser240 residue in the C-terminal region of the 40S ribosomal protein S6 (RPS6). These results were confirmed by Western blot analysis using an antibody that specifically recognizes phosphorylated Ser240 in RPS6. Finally, this antibody was used to follow TOR activity in plants. Our results thus uncover a multi-level regulation of plant ribosomal genes and proteins by the TOR kinase.

  • 8.
    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.

  • 9. Ferrando, Alejandro
    et al.
    Mar Castellano, M.
    Lison, Purificacion
    Leister, Dario
    Stepanova, Anna N.
    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.
    Editorial: Relevance of Translational Regulation on Plant Growth and Environmental Responses2017In: Frontiers in Plant Science, ISSN 1664-462X, E-ISSN 1664-462X, Vol. 8, article id 2170Article in journal (Other academic)
  • 10. Gamm, Magdalena
    et al.
    Peviani, Alessia
    Honsel, Anne
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Snel, Berend
    Smeekens, Sjef
    Hanson, Johannes
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Increased sucrose levels mediate selective mRNA translation in Arabidopsis2014In: BMC Plant Biology, ISSN 1471-2229, E-ISSN 1471-2229, Vol. 14, article id 306Article in journal (Refereed)
    Abstract [en]

    Background: Protein synthesis is a highly energy demanding process and is regulated according to cellular energy levels. Light and sugar availability affect mRNA translation in plant cells but the specific roles of these factors remain unclear. In this study, sucrose was applied to Arabidopsis seedlings kept in the light or in the dark, in order to distinguish sucrose and light effects on transcription and translation. These were studied using microarray analysis of steady-state mRNA and mRNA bound to translating ribosomes. Results: Steady-state mRNA levels were affected differently by sucrose in the light and in the dark but general translation increased to a similar extent in both conditions. For a majority of the transcripts changes of the transcript levels were followed by changes in polysomal mRNA levels. However, for 243 mRNAs, a change in polysomal occupancy (defined as polysomal levels related to steady-state levels of the mRNA) was observed after sucrose treatment in the light, but not in the dark condition. Many of these mRNAs are annotated as encoding ribosomal proteins, supporting specific translational regulation of this group of transcripts. Unexpectedly, the numbers of ribosomes bound to each mRNA decreased for mRNAs with increased polysomal occupancy. Conclusions: Our results suggest that sucrose regulate translation of these 243 mRNAs specifically in the light, through a novel regulatory mechanism. Our data shows that increased polysomal occupancy is not necessarily leading to more ribosomes per transcript, suggesting a mechanism of translational induction not solely dependent on increased translation initiation rates.

  • 11.
    Hanson, Johannes
    et al.
    Department of Molecular Plant Physiology, Utrecht University, NL-3584 CH Utrecht, The Netherlands.
    Hanssen, Micha
    Molecular Plant Physiology, Utrecht University, Utrecht, The Netherlands.
    Wiese, Anika
    Molecular Plant Physiology, Utrecht University, Utrecht, The Netherlands.
    Hendriks, Margriet M W B
    ABC Metabolomics Centre, Utrecht University, Utrecht, The Netherlands.
    Smeekens, Sjef
    Molecular Plant Physiology, Utrecht University, Utrecht, The Netherlands.
    The sucrose regulated transcription factor bZIP11 affects amino acid metabolism by regulating the expression of ASPARAGINE SYNTHETASE1 and PROLINE DEHYDROGENASE22008In: The Plant Journal, ISSN 0960-7412, E-ISSN 1365-313X, Vol. 53, no 6, p. 935-949Article in journal (Refereed)
    Abstract [en]

    Translation of the transcription factor bZIP11 is repressed by sucrose in a process that involves a highly conserved peptide encoded by the 5' leaders of bZIP11 and other plant basic region leucine zipper (bZip) genes. It is likely that a specific signaling pathway operating at physiological sucrose concentrations controls metabolism via a feedback mechanism. In this paper bZIP11 target processes are identified using transiently increased nuclear bZIP11 levels and genome-wide expression analysis. bZIP11 affects the expression of hundreds of genes with proposed functions in biochemical pathways and signal transduction. The expression levels of approximately 80% of the genes tested are not affected by bZIP11 promoter-mediated overexpression of bZIP11. This suggests that <20% of the identified genes appear to be physiologically relevant targets of bZIP11. ASPARAGINE SYNTHETASE1 and PROLINE DEHYDROGENASE2 are among the rapidly activated bZIP11 targets, whose induction is independent of protein translation. Transient expression experiments in Arabidopsis protoplasts show that the bZIP11-dependent activation of the ASPARAGINE SYNTHETASE1 gene is dependent on a G-box element present in the promoter. Increased bZIP11 expression leads to decreased proline and increased phenylalanine levels. A model is proposed in which sugar signals control amino acid levels via the bZIP11 transcription factor.

  • 12.
    Hanson, Johannes
    et al.
    Department of Physiological Botany, Evolutionary Biology Center, Uppsala University, Uppsala, Sweden.
    Johannesson, Henrik
    Department of Physiological Botany, Evolutionary Biology Center, Uppsala University, Uppsala, Sweden.
    Engström, Peter
    Department of Physiological Botany, Evolutionary Biology Center, Uppsala University, Uppsala, Sweden.
    Sugar-dependent alterations in cotyledon and leaf development in transgenic plants expressing the HDZhdip gene ATHB132001In: Plant Molecular Biology, ISSN 0167-4412, E-ISSN 1573-5028, Vol. 45, no 3, p. 247-262Article in journal (Refereed)
    Abstract [en]

    ATHB13 is a new member of the homeodomain leucine zipper (HDZip) transcription factor family of Arabidopsis thaliana. Constitutive high-level expression of the ATHB13 cDNA in transgenic plants results in altered development of cotyledons and leaves, specifically in plants grown on media containing metabolizable sugars. Cotyledons and leaves of sugar-grown transgenic plants are more narrow and the junction between the petiole and the leaf blade less distinct, as compared to the wild type. High-level expression of ATHB13 affects cotyledon shape by inhibiting lateral expansion of epidermal cells in sugar-treated seedlings. Experiments with non-metabolizable sugars indicate that the alteration in leaf shape in the ATHB13 transgenics is mediated by sucrose sensing. ATHB13 further affects a subset of the gene expression responses of the wild-type plant to sugars. The expression of genes encoding beta-amylase and vegetative storage protein is induced to higher levels in response to sucrose in the transgenic plants as compared to the wild type. The expression of other sugar-regulated genes examined is unaffected by ATHB13. These data suggest that ATHB13 may be a component of the sucrose-signalling pathway, active close to the targets of the signal transduction.

  • 13.
    Hanson, Johannes
    et al.
    Department of Physiological Botany, Evolutionary Biology Center, University of Uppsala.
    Regan, S.
    Engström, P.
    The expression pattern of the homeobox gene ATHB13 reveals a conservation of transcriptional regulatory mechanisms between Arabidopsis and hybrid aspen2002In: Plant Cell Reports, ISSN 0721-7714, E-ISSN 1432-203X, Vol. 21, no 1, p. 81-89Article in journal (Refereed)
    Abstract [en]

    ATHB13 belongs to a family of homeodomain leucine zipper (HDZip) transcription factors in Arabidopsis thaliana. To understand the temporal and spatial distribution of ATHB13 gene expression, we examined the ATHB13 promoter activity by means of fusions to the uidA (GUS, beta-glucuronidase) reporter gene in transgenic plants. The strongest promoter activity was detected in the vasculature of the basal portion of petioles for both rosette leaves and cotyledons and at the base of cauline leaves. Activity was also detected in the stem at the base of the cauline leaf in an area corresponding to the leaf gap in the vasculature. In flowers, promoter activity was also present in the receptacle and in the stigma. Transformation of the same promoter-GUS construct into hybrid aspen (Populus tremula x P. tremuloides) resulted in an analogous expression pattern in the petioles of leaves. The similarity of these expression patterns indicates that the trans-acting factors responsible for ATHB13 expression are conserved between aspen and Arabidopsis. The conserved expression pattern of the highly specific Arabidopsis ATHB13 promoter in hybrid aspen demonstrates the potential utility of Arabidopsis promoters for tissue-specific expression in angiosperm trees.

  • 14.
    Hanson, Johannes
    et al.
    Molecular Plant Physiology, Utrecht University, Utrecht, The Netherlands; Centre for BioSystems Genomics, Wageningen, The Netherlands.
    Smeekens, Sjef
    Molecular Plant Physiology, Utrecht University, Utrecht, The Netherlands; Centre for BioSystems Genomics, Wageningen, The Netherlands.
    Sugar perception and signaling: an update2009In: Current opinion in plant biology, ISSN 1369-5266, E-ISSN 1879-0356, Vol. 12, no 5, p. 562-567Article in journal (Refereed)
    Abstract [en]

    Sugars act as potent signaling molecules in plants. Several sugar sensors, including the highly studied glucose sensor HEXOKINASE1 (HXK1), have been identified or proposed. Many additional sensors likely exist, as plants respond to other sugars and sugar metabolites, such as sucrose and trehalose 6-phosphate. Sugar sensing and signaling is a highly complex process resulting in many changes in physiology and development and is integrated with other signaling pathways in plants such as those for inorganic nutrients, hormones, and different stress factors. Importantly, KIN10 and KIN11 protein kinases are central in coordinating several of the responses to sugars and stress. bZIP transcription factors were found to mediate effects of sugar signaling on gene expression and metabolite content.

  • 15. Hartmann, Laura
    et al.
    Pedrotti, Lorenzo
    Weiste, Christoph
    Fekete, Agnes
    Schierstaedt, Jasper
    Göttler, Jasmin
    Kempa, Stefan
    Krischke, Markus
    Dietrich, Katrin
    Mueller, Martin J
    Vicente-Carbajosa, Jesus
    Hanson, Johannes
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC). Department of Molecular Plant Physiology, Utrecht University, The Netherlands .
    Dröge-Laser, Wolfgang
    Crosstalk between Two bZIP Signaling Pathways Orchestrates Salt-Induced Metabolic Reprogramming in Arabidopsis Roots2015In: The Plant Cell, ISSN 1040-4651, E-ISSN 1532-298X, Vol. 27, no 8, p. 2244-2260Article in journal (Refereed)
    Abstract [en]

    Soil salinity increasingly causes crop losses worldwide. Although roots are the primary targets of salt stress, the signaling networks that facilitate metabolic reprogramming to induce stress tolerance are less understood than those in leaves. Here, a combination of transcriptomic and metabolic approaches was performed in salt-treated Arabidopsis thaliana roots, which revealed that the group S1 basic leucine zipper transcription factors bZIP1 and bZIP53 reprogram primary C- and N-metabolism. In particular, gluconeogenesis and amino acid catabolism are affected by these transcription factors. Importantly, bZIP1 expression reflects cellular stress and energy status in roots. In addition to the well-described abiotic stress response pathway initiated by the hormone abscisic acid (ABA) and executed by SnRK2 (Snf1-RELATED-PROTEIN-KINASE2) and AREB-like bZIP factors, we identify a structurally related ABA-independent signaling module consisting of SnRK1s and S1 bZIPs. Crosstalk between these signaling pathways recruits particular bZIP factor combinations to establish at least four distinct gene expression patterns. Understanding this signaling network provides a framework for securing future crop productivity.

  • 16. He, Hanzi
    et al.
    Willems, Leo
    Batushansky, Albert
    Fait, Aaron
    Hanson, Johannes
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC). Department of Molecular Plant Physiology, Utrecht University, NL-3584 CH Utrecht, The Netherlands.
    Nijveen, Harm
    Hilhorst, Henk W M
    Bentsink, Leónie
    Effects of Parental Temperature and Nitrate on Seed Performance are Reflected by Partly Overlapping Genetic and Metabolic Pathways2016In: Plant and Cell Physiology, ISSN 0032-0781, E-ISSN 1471-9053, Vol. 57, no 3, p. 473-487Article in journal (Refereed)
    Abstract [en]

    Seed performance is affected by the seed maturation environment and previously, we have shown that temperature, nitrate and light intensity were the most influential environmental factors affecting seed performance. Seeds developed in these environments were selected to assess the underlying metabolic pathways, using a combination of transcriptomics and metabolomics. These analyses revealed that the effects of the temperature and nitrate parental environments were reflected by partly overlapping genetic and metabolic networks, as indicated by similar changes in metabolites and transcripts expression levels. Nitrogen-metabolism related metabolites (asparagine, GABA and allantoin) were significantly decreased in both low temperature (15°C) and low nitrate (N0) maturation environments. Correspondingly, nitrogen-metabolism genes (ALLANTOINASE, NITRATE REDUCTASE 1, NITRITE REDUCTASE 1 and NITRILASE 4) were differentially regulated in the low temperature and nitrate maturation environments, as compared with control conditions. High light intensity during seed maturation increased galactinol content, and displayed a high correlation with seed longevity. Low light had a genotype-specific effect on cell surface encoding genes in the DELAY OF GERMINATION 6-Near Isogenic Line (NILDOG6). Overall, the integration of phenotypes, metabolites and transcripts led to new insights in the regulation of seed performance.

  • 17.
    Henriksson, Eva
    et al.
    Turku Centre for Biotechnology, University of Turku, Åbo Academy University, Turku, Finland; Department of Physiological Botany, Evolutionary Biology Centre, University of Uppsala, Uppsala, Sweden.
    Olsson, Anna S B
    Department of Physiological Botany, Evolutionary Biology Centre, University of Uppsala, Uppsala, Sweden.
    Johannesson, Henrik
    Department of Physiological Botany, Evolutionary Biology Centre, University of Uppsala, Uppsala, Sweden.
    Johansson, Henrik
    Department of Physiological Botany, Evolutionary Biology Centre, University of Uppsala, Uppsala, Sweden.
    Hanson, Johannes
    Department of Physiological Botany, Evolutionary Biology Centre, University of Uppsala, Uppsala, Sweden; Department of Molecular Plant Physiology, Utrecht University, NL-3584 CH Utrecht, The Netherlands.
    Engström, Peter
    Department of Physiological Botany, Evolutionary Biology Centre, University of Uppsala, Uppsala, Sweden.
    Söderman, Eva
    Department of Physiological Botany, Evolutionary Biology Centre, University of Uppsala, Uppsala, Sweden.
    Homeodomain leucine zipper class I genes in Arabidopsis. Expression patterns and phylogenetic relationships2005In: Plant Physiology, ISSN 0032-0889, E-ISSN 1532-2548, Vol. 139, no 1, p. 509-518Article in journal (Refereed)
    Abstract [en]

    Members of the homeodomain leucine zipper (HDZip) family of transcription factors are present in a wide range of plants, from mosses to higher plants, but not in other eukaryotes. The HDZip genes act in developmental processes, including vascular tissue and trichome development, and several of them have been suggested to be involved in the mediation of external signals to regulate plant growth. The Arabidopsis (Arabidopsis thaliana) genome contains 47 HDZip genes, which, based on sequence criteria, have been grouped into four different classes: HDZip I to IV. In this article, we present an overview of the class I HDZip genes in Arabidopsis. We describe their expression patterns, transcriptional regulation properties, duplication history, and phylogeny. The phylogeny of HDZip class I genes is supported by data on the duplication history of the genes, as well as the intron/exon patterning of the HDZip-encoding motifs. The HDZip class I genes were found to be widely expressed and partly to have overlapping expression patterns at the organ level. Further, abscisic acid or water deficit treatments and different light conditions affected the transcript levels of a majority of the HDZip I genes. Within the gene family, our data show examples of closely related HDZip genes with similarities in the function of the gene product, but a divergence in expression pattern. In addition, six HDZip class I proteins tested were found to be activators of gene expression. In conclusion, several HDZip I genes appear to regulate similar cellular processes, although in different organs or tissues and in response to different environmental signals.

  • 18. Hummel, Maureen
    et al.
    Cordewener, Jan H. G.
    de Groot, Joost C. M.
    Smeekens, Sjef
    America, Antoine H. P.
    Hanson, Johannes
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Dynamic protein composition of Arabidopsis thaliana cytosolic ribosomes in response to sucrose feeding as revealed by label free MSE proteomics2012In: Proteomics, ISSN 1615-9853, E-ISSN 1615-9861, Vol. 12, no 7, p. 1024-1038Article in journal (Refereed)
    Abstract [en]

    Cytosolic ribosomes are among the largest multisubunit cellular complexes. Arabidopsis thaliana ribosomes consist of 79 different ribosomal proteins (r-proteins) that each are encoded by two to six (paralogous) genes. It is unknown whether the paralogs are incorporated into the ribosome and whether the relative incorporation of r-protein paralogs varies in response to environmental cues. Immunopurified ribosomes were isolated from A. thaliana rosette leaves fed with sucrose. Trypsin digested samples were analyzed by qTOF-LC-MS using both MSE and classical MS/MS. Peptide features obtained by using these two methods were identified using MASCOT and Proteinlynx Global Server searching the theoretical sequences of A. thaliana proteins. The A. thaliana genome encodes 237 r-proteins and 69% of these were identified with proteotypic peptides for most of the identified proteins. These r-proteins were identified with average protein sequence coverage of 32% observed by MSE. Interestingly, the analysis shows that the abundance of r-protein paralogs in the ribosome changes in response to sucrose feeding. This is particularly evident for paralogous RPS3aA, RPS5A, RPL8B, and RACK1 proteins. These results show that protein synthesis in the A. thaliana cytosol involves a heterogeneous ribosomal population. The implications of these findings in the regulation of translation are discussed.

  • 19. Hummel, Maureen
    et al.
    Dobrenel, Thomas
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Institut Jean-Pierre Bourgin, UMR 1318 INRA AgroParisTech, Saclay Plant Sciences, F-78026 Versailles, France.
    Cordewener, Jan (J. H. G)
    Davanture, Marlene
    Meyer, Christian
    Smeekens, Sjef (J. C. M)
    Bailey-Serres, Julia
    America, Twan (A. H. P)
    Hanson, Johannes
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Molecular Plant Physiology, Utrecht University, Padualaan 8, 3584 CH, Utrecht, The Netherlands.
    Proteomic LC-MS analysis of Arabidopsis cytosolic ribosomes: Identification of ribosomal protein paralogs and re-annotation of the ribosomal protein genes2015In: Journal of Proteomics, ISSN 1874-3919, E-ISSN 1876-7737, Vol. 128, p. 436-449Article in journal (Refereed)
    Abstract [en]

    Arabidopsis thaliana cytosolic ribosomes are large complexes containing eighty-one distinct ribosomal proteins (r-proteins), four ribosomal RNAs (rRNA) and a plethora of associated (non-ribosomal) proteins. In plants, r-proteins of cytosolic ribosomes are each encoded by two to seven different expressed and similar genes, forming an r-protein family. 

    Distinctions in the r-protein coding sequences of gene family members are a source of variation between ribosomes. We performed proteomic investigation of actively translating cytosolic ribosomes purified using both immunopurification and a classic sucrose cushion centrifugation-based protocol from plants of different developmental stages. Both 1D and 2D LC MSE with data-independent acquisition as well as conventional data-dependent MS/MS procedures were applied. This approach provided detailed identification of 165 r-protein paralogs with high coverage based on proteotypic peptides. The detected r-proteins were the products of the majority (68%) of the 242 cytosolic r-protein genes encoded by the genome. A total of 70 distinct r-proteins were identified. Based on these results and information from DNA microarray and ribosome footprint profiling studies a re-annotation of Arabidopsis r-proteins and genes is proposed. This compendium of the cytosolic r-protein proteome will serve as a template for future investigations on the dynamic structure and function of plant ribosomes. 

    Biological significance: Translation is one of the most energy demanding processes in a living cell and is therefore carefully regulated. Translational activity is tightly linked to growth control and growth regulating mechanism. Recently established translational profiling technologies, including the profiling of mRNAs associated with polysomes and the mapping of ribosome footprints on mRNAs, have revealed that the expression of gene expression is often fine-tuned by differential translation of gene transcripts. The eukaryotic ribosome, the hub of these important processes, consists of close to eighty different proteins (depending on species) and four large RNAs assembled into two highly conserved subunits. 

    In plants and to lesser extent in yeast the r-proteins are encoded by more than one actively transcribed gene. As r-protein gene paralogs frequently do not encode identical proteins and are regulated by growth conditions and development, in vivo ribosomes are heterogeneous in their protein content The regulatory and physiological importance of this heterogeneity is unknown. Here, an improved annotation of the more than two hundred r-protein genes of Arabidopsis is presented that combines proteomic and advanced mRNA expression data. This proteomic investigation and re-annotation of Arabidopsis ribosomes establish a base for future investigations of translational control in plants.

  • 20.
    Hummel, Maureen
    et al.
    Molecular Plant Physiology, Utrecht University, Utrecht, The Netherlands.
    Rahmani, Fatima
    Molecular Plant Physiology, Utrecht University, Utrecht, The Netherlands.
    Smeekens, Sjef
    Molecular Plant Physiology, Utrecht University, Utrecht, The Netherlands; Centre for BioSystems Genomics, Wageningen, The Netherlands.
    Hanson, Johannes
    Molecular Plant Physiology, Utrecht University, Utrecht, The Netherlands; Centre for BioSystems Genomics, Wageningen, The Netherlands.
    Sucrose-mediated translational control2009In: Annals of Botany, ISSN 0305-7364, E-ISSN 1095-8290, Vol. 104, no 1, p. 1-7Article in journal (Refereed)
    Abstract [en]

    BACKGROUND: Environmental factors greatly impact plant gene expression and concentrations of cellular metabolites such as sugars and amino acids. The changed metabolite concentrations affect the expression of many genes both transcriptionally and post-transcriptionally.

    RECENT PROGRESS: Sucrose acts as a signalling molecule in the control of translation of the S1 class basic leucine zipper transcription factor (bZIP) genes. In these genes the main bZIP open reading frames (ORFs) are preceded by upstream open reading frames (uORFs). The presence of uORFs generally inhibits translation of the following ORF but can also be instrumental in specific translational control. bZIP11, a member of the S1 class bZIP genes, harbours four uORFs of which uORF2 is required for translational control in response to sucrose concentrations. This uORF encodes the Sucrose Control peptide (SC-peptide), which is evolutionarily conserved among all S1 class bZIP genes in different plant species. Arabidopsis thaliana bZIP11 and related bZIP genes seem to be important regulators of metabolism. These proteins are targets of the Snf1-related protein kinase 1 (SnRK1) KIN10 and KIN11, which are responsive to energy deprivation as well as to various stresses. In response to energy deprivation, ribosomal biogenesis is repressed to preserve cellular function and maintenance. Other key regulators of ribosomal biogenesis such as the protein kinase Target of Rapamycin (TOR) are tightly regulated in response to stress.

    CONCLUSIONS: Plants use translational control of gene expression to optimize growth and development in response to stress as well as to energy deprivation. This Botanical Briefing discusses the role of sucrose signalling in the translational control of bZIP11 and the regulation of ribosomal biogenesis in response to metabolic changes and stress conditions.

  • 21.
    Johannesson, Henrik
    et al.
    ary Biology Center, Department of Physiological Botany, Uppsala, Sweden.
    Wang, Yan
    Department of Physiological Botany, Evolutionary Biology Center, Uppsala, Sweden.
    Hanson, Johannes
    Department of Physiological Botany, Evolutionary Biology Center, Uppsala, Sweden.
    Engström, Peter
    Department of Physiological Botany, Evolutionary Biology Center, Uppsala, Sweden.
    The Arabidopsis thaliana homeobox gene ATHB5 is a potential regulator of abscisic acid responsiveness in developing seedlings2003In: Plant Molecular Biology, ISSN 0167-4412, E-ISSN 1573-5028, Vol. 51, no 5, p. 719-729Article in journal (Refereed)
    Abstract [en]

    ATHB5 is a member of the homeodomain-leucine zipper (HDZip) transcription factor gene family of Arabidopsis thaliana. In this report we show that increased expression levels of ATHB5 in transgenic Arabidopsis plants cause an enhanced sensitivity to the inhibitory effect of abscisic acid (ABA) on seed germination and seedling growth. Consistent with this finding we demonstrate in northern blot experiments that the ABA-responsive gene RAB18 is hyperinduced by ABA in transgenic overexpressor lines as compared to the wild type. Northern blot and promoter-GUS fusion analyses show that ATHB5 gene transcription is initiated rapidly after the onset of germination and localized primarily to the hypocotyl of germinating seedlings. Moreover, analysis of ATHB5 gene expression during post-germinative growth in different ABA response mutants shows that ATHB5 gene activity is down-regulated in the abil-1, abi3-1 and abi5-1 mutant lines, but not in abi2-1 or abi4-1. The identification of a T-DNA insertion mutant line of ATHB5 is described and no phenotypic alterations could be discerned, suggesting that ATHB5 may act redundantly with other HDZip genes. Taken together, these data suggest that ATHB5 is a positive regulator of ABA-responsiveness, mediating the inhibitory effect of ABA on growth during seedling establishment.

  • 22.
    Lastdrager, Jeroen
    et al.
    Molecular Plant Physiology, Institute of Environmental Biology, Utrecht University, Padualaan 8, 3584 CH Utrecht, The Netherlands .
    Hanson, Johannes
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Molecular Plant Physiology, Institute of Environmental Biology, Utrecht University, Padualaan 8, 3584 CH Utrecht, The Netherlands.
    Smeekens, Sjef
    Molecular Plant Physiology, Institute of Environmental Biology, Utrecht University, Padualaan 8, 3584 CH Utrecht, The Netherlands.
    Sugar signals and the control of plant growth and development2014In: Journal of Experimental Botany, ISSN 0022-0957, E-ISSN 1460-2431, Vol. 65, no 3, p. 799-807Article, review/survey (Refereed)
    Abstract [en]

    Sugars are key regulators that control plant growth and development, including biomass accumulation. Major sugar-responsive signalling systems are reviewed, with emphasis on trehalose 6-phosphate, TOR kinase, SnRK1, and the C/S1-bZIP network.Sugars have a central regulatory function in steering plant growth. This review focuses on information presented in the past 2 years on key players in sugar-mediated plant growth regulation, with emphasis on trehalose 6-phosphate, target of rapamycin kinase, and Snf1-related kinase 1 regulatory systems. The regulation of protein synthesis by sugars is fundamental to plant growth control, and recent advances in our understanding of the regulation of translation by sugars will be discussed.

  • 23. Li, Ping
    et al.
    Wind, Julia J
    Shi, Xiaoliang
    Zhang, Honglei
    Hanson, Johannes
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Smeekens, Sjef C
    Teng, Sheng
    Fructose sensitivity is suppressed in Arabidopsis by the transcription factor ANAC089 lacking the membrane-bound domain2011In: Proceedings of the National Academy of Sciences of the United States of America, ISSN 0027-8424, E-ISSN 1091-6490, Vol. 108, no 8, p. 3436-3441Article in journal (Refereed)
    Abstract [en]

    In living organisms sugars not only provide energy and carbon skeletons but also act as evolutionarily conserved signaling molecules. The three major soluble sugars in plants are sucrose, glucose, and fructose. Information on plant glucose and sucrose signaling is available, but to date no fructose-specific signaling pathway has been reported. In this study, sugar repression of seedling development was used to study fructose sensitivity in the Landsberg erecta (Ler)/Cape Verde Islands (Cvi) recombinant inbred line population, and eight fructose-sensing quantitative trait loci (QTLs) (FSQ1-8) were mapped. Among them, FSQ6 was confirmed to be a fructose-specific QTL by analyzing near-isogenic lines in which Cvi genomic fragments were introgressed in the Ler background. These results indicate the existence of a fructose-specific signaling pathway in Arabidopsis. Further analysis demonstrated that the FSQ6-associated fructose-signaling pathway functions independently of the hexokinase1 (HXK1) glucose sensor. Remarkably, fructose-specific FSQ6 downstream signaling interacts with abscisic acid (ABA)- and ethylene-signaling pathways, similar to HXK1-dependent glucose signaling. The Cvi allele of FSQ6 acts as a suppressor of fructose signaling. The FSQ6 gene was identified using map-based cloning approach, and FSQ6 was shown to encode the transcription factor gene Arabidopsis NAC (petunia No apical meristem and Arabidopsis transcription activation factor 1, 2 and Cup-shaped cotyledon 2) domain containing protein 89 (ANAC089). The Cvi allele of FSQ6/ANAC089 is a gain-of-function allele caused by a premature stop in the third exon of the gene. The truncated Cvi FSQ6/ANAC089 protein lacks a membrane association domain that is present in ANAC089 proteins from other Arabidopsis accessions. As a result, Cvi FSQ6/ANAC089 is constitutively active as a transcription factor in the nucleus.

  • 24. Ma, Jingkun
    et al.
    Hanssen, Micha
    Lundgren, Krister
    Hernández, Lázaro
    Delatte, Thierry
    Ehlert, Andrea
    Liu, Chun-Ming
    Schluepmann, Henriette
    Dröge-Laser, Wolfgang
    Moritz, Thomas
    Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Smeekens, Sjef
    Hanson, Johannes
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    The sucrose-regulated Arabidopsis transcription factor bZIP11 reprograms metabolism and regulates trehalose metabolism2011In: New Phytologist, ISSN 0028-646X, E-ISSN 1469-8137, Vol. 191, no 3, p. 733-745Article in journal (Refereed)
    Abstract [en]

    • The Arabidopsis basic region-leucine zipper transcription factor 11 (bZIP11) is known to be repressed by sucrose through a translational inhibition mechanism that requires the conserved sucrose control peptide encoded by the mRNA leader. The function of bZIP11 has been investigated in over-expression studies, and bZIP11 has been found to inhibit plant growth. The addition of sugar does not rescue the growth inhibition phenotype. Here, the function of the bZIP11 transcription factor was investigated. • The mechanism by which bZIP11 regulates growth was studied using large-scale and dedicated metabolic analysis, biochemical assays and molecular studies. • bZIP11 induction results in a reprogramming of metabolism and activation of genes involved in the metabolism of trehalose and other minor carbohydrates such as myo-inositol and raffinose. bZIP11 induction leads to reduced contents of the prominent growth regulatory molecule trehalose 6-phosphate (T6P). • The metabolic changes detected mimic in part those observed in carbon-starved plants. It is proposed that bZIP11 is a powerful regulator of carbohydrate metabolism that functions in a growth regulatory network that includes T6P and the sucrose non-fermenting-1 related protein kinase 1 (SnRK1).

  • 25.
    Mair, Andrea
    et al.
    Vienna, Austria.
    Pedrotti, Lorenzo
    Würzburg, Germany.
    Wurzinger, Bernhard
    Vienna, Austria.
    Anrather, Dorothea
    Vienna, Austria.
    Simeunovic, Andrea
    Vienna, Austria.
    Weiste, Christoph
    Würzburg, Germany.
    Valerio, Concetta
    Oeiras, Portugal.
    Dietrich, Katrin
    Würzburg, Germany.
    Kirchler, Tobias
    Tübingen, Germany.
    Nägele, Thomas
    Vienna, Austria.
    Vicente Carbajosa, Jesús
    Madrid, Spain.
    Hanson, Johannes
    Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC). Molecular Plant Physiology, Utrecht University, Utrecht, The Netherlands.
    Baena-González, Elena
    Oeiras, Portugal.
    Chaban, Christina
    Tübingen, Germany.
    Weckwerth, Wolfram
    Vienna, Austria.
    Dröge-Laser, Wolfgang
    Würzburg, Germany.
    Teige, Markus
    Vienna, Austria.
    SnRK1-triggered switch of bZIP63 dimerization mediates the low-energy response in plants2015In: eLIFE, E-ISSN 2050-084X, Vol. 4, article id e05828Article in journal (Refereed)
    Abstract [en]

    Metabolic adjustment to changing environmental conditions, particularly balancing of growth and defense responses, is crucial for all organisms to survive. The evolutionary conserved AMPK/Snf1/SnRK1 kinases are well-known metabolic master regulators in the low-energy response in animals, yeast and plants. They act at two different levels: by modulating the activity of key metabolic enzymes, and by massive transcriptional reprogramming. While the first part is well established, the latter function is only partially understood in animals and not at all in plants. Here we identified the Arabidopsis transcription factor bZIP63 as key regulator of the starvation response and direct target of the SnRK1 kinase. Phosphorylation of bZIP63 by SnRK1 changed its dimerization preference, thereby affecting target gene expression and ultimately primary metabolism. A bzip63 knock-out mutant exhibited starvation-related phenotypes, which could be functionally complemented by wild type bZIP63, but not by a version harboring point mutations in the identified SnRK1 target sites.

  • 26. Nukarinen, Ella
    et al.
    Nägele, Thomas
    Pedrotti, Lorenzo
    Wurzinger, Bernhard
    Mair, Andrea
    Landgraf, Ramona
    Börnke, Frederik
    Hanson, Johannes
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology.
    Teige, Markus
    Baena-Gonzalez, Elena
    Dröge-Laser, Wolfgang
    Weckwerth, Wolfram
    Quantitative phosphoproteomics reveals the role of the AMPK plant ortholog SnRK1 as a metabolic master regulator under energy deprivation2016In: Scientific Reports, ISSN 2045-2322, E-ISSN 2045-2322, Vol. 6, article id 31697Article in journal (Refereed)
    Abstract [en]

    Since years, research on SnRK1, the major cellular energy sensor in plants, has tried to define its role in energy signalling. However, these attempts were notoriously hampered by the lethality of a complete knockout of SnRK1. Therefore, we generated an inducible amiRNA::SnRK1α2 in a snrk1α1 knock out background (snrk1α1/α2) to abolish SnRK1 activity to understand major systemic functions of SnRK1 signalling under energy deprivation triggered by extended night treatment. We analysed the in vivo phosphoproteome, proteome and metabolome and found that activation of SnRK1 is essential for repression of high energy demanding cell processes such as protein synthesis. The most abundant effect was the constitutively high phosphorylation of ribosomal protein S6 (RPS6) in the snrk1α1/α2 mutant. RPS6 is a major target of TOR signalling and its phosphorylation correlates with translation. Further evidence for an antagonistic SnRK1 and TOR crosstalk comparable to the animal system was demonstrated by the in vivo interaction of SnRK1α1 and RAPTOR1B in the cytosol and by phosphorylation of RAPTOR1B by SnRK1α1 in kinase assays. Moreover, changed levels of phosphorylation states of several chloroplastic proteins in the snrk1α1/α2 mutant indicated an unexpected link to regulation of photosynthesis, the main energy source in plants.

  • 27. Peviani, Alessia
    et al.
    Lastdrager, Jeroen
    Hanson, Johannes
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC). Molecular Plant Physiology, Institute of Environmental Biology, Utrecht University, Utrecht, The Netherlands.
    Snel, Berend
    The phylogeny of C/S1 bZIP transcription factors reveals a shared algal ancestry and the pre-angiosperm translational regulation of S1 transcripts2016In: Scientific Reports, ISSN 2045-2322, E-ISSN 2045-2322, Vol. 6, article id 30444Article in journal (Refereed)
    Abstract [en]

    Basic leucine zippers (bZIPs) form a large plant transcription factor family. C and S1 bZIP groups can heterodimerize, fulfilling crucial roles in seed development and stress response. S1 sequences also harbor a unique regulatory mechanism, termed Sucrose-Induced Repression of Translation (SIRT). The conservation of both C/S1 bZIP interactions and SIRT remains poorly characterized in non-model species, leaving their evolutionary origin uncertain and limiting crop research. In this work, we explored recently published plant sequencing data to establish a detailed phylogeny of C and S1 bZIPs, investigating their intertwined role in plant evolution, and the origin of SIRT. Our analyses clarified C and S1 bZIP orthology relationships in angiosperms, and identified S1 sequences in gymnosperms. We experimentally showed that the gymnosperm orthologs are regulated by SIRT, tracing back the origin of this unique regulatory mechanism to the ancestor of seed plants. Additionally, we discovered an earlier S ortholog in the charophyte algae Klebsormidium flaccidum, together with a C ortholog. This suggests that C and S groups originated by duplication from a single algal proto-C/S ancestor. Based on our observations, we propose a model wherein the C/S1 bZIP dimer network evolved in seed plants from pre-existing C/S bZIP interactions.

  • 28.
    Rahmani, Fatemeh
    et al.
    Molecular Plant Physiology, Utrecht University, Utrecht, The Netherlands; Centre for BioSystems Genomics, Wageningen, The Netherlands.
    Hummel, Maureen
    Molecular Plant Physiology, Utrecht University, Utrecht, The Netherlands; Centre for BioSystems Genomics, Wageningen, The Netherlands.
    Schuurmans, Jolanda
    Molecular Plant Physiology, Utrecht University, Utrecht, The Netherlands; Centre for BioSystems Genomics, Wageningen, The Netherlands.
    Wiese-Klinkenberg, Anika
    Molecular Plant Physiology, Utrecht University, Utrecht, The Netherlands; Centre for BioSystems Genomics, Wageningen, The Netherlands.
    Smeekens, Sjef
    Molecular Plant Physiology, Utrecht University, Utrecht, The Netherlands; Centre for BioSystems Genomics, Wageningen, The Netherlands.
    Hanson, Johannes
    Molecular Plant Physiology, Utrecht University, Utrecht, The Netherlands; Centre for BioSystems Genomics, Wageningen, The Netherlands.
    Sucrose control of translation mediated by an upstream open reading frame-encoded peptide2009In: Plant Physiology, ISSN 0032-0889, E-ISSN 1532-2548, Vol. 150, no 3, p. 1356-1367Article in journal (Refereed)
    Abstract [en]

    Regulation of gene expression through translational control is common in many organisms. The Arabidopsis (Arabidopsis thaliana) transcription factor bZIP11 is translational repressed in response to sucrose (Suc), resulting in Suc-regulated changes in amino acid metabolism. The 5' leader of the bZIP11 mRNA harbors several upstream open reading frames (uORFs), of which the second uORF is well conserved among bZIP11 homologous genes. The uORF2 element encodes a Suc control peptide (SC-peptide) of 28 residues that is sufficient for imposing Suc-induced repression of translation (SIRT) on a heterologous mRNA. Detailed analysis of the SC-peptide suggests that it functions as an attenuator peptide. Results suggest that the SC-peptide inhibits bZIP11 translation in response to high Suc levels by stalling the ribosome on the mRNA. The conserved noncanonical AUG contexts of bZIP11 uORFs allow inefficient translational initiation of the uORF, resulting in translation initiation of the scanning ribosome at the AUG codon of the bZIP11 main ORF. The results presented show that Suc-dependent signaling mediates differential translation of mRNAs containing SC-peptides encoding uORFs.

  • 29.
    Smeekens, Sjef
    et al.
    Molecular Plant Physiology, Utrecht University, Utrecht, The Netherlands; Centre for BioSystems Genomics, Wageningen, The Netherlands.
    Ma, Jingkun
    Molecular Plant Physiology, Utrecht University, Utrecht, The Netherlands; Beijing, China.
    Hanson, Johannes
    Molecular Plant Physiology, Utrecht University, Utrecht, The Netherlands; Centre for BioSystems Genomics, Wageningen, The Netherlands.
    Rolland, Filip
    Leuven-Heverlee, Belgium.
    Sugar signals and molecular networks controlling plant growth2010In: Current opinion in plant biology, ISSN 1369-5266, E-ISSN 1879-0356, Vol. 13, no 3, p. 274-279Article in journal (Refereed)
    Abstract [en]

    In recent years, several regulatory systems that link carbon nutrient status to plant growth and development have emerged. In this paper, we discuss the growth promoting functions of the hexokinase (HXK) glucose sensor, the trehalose 6-phosphate (T6P) signal and the Target of Rapamycin (TOR) kinase pathway, and the growth inhibitory function of the SNF1-related Protein Kinase1 (SnRK1) and the C/S1 bZIP transcription factor network. It is crucial that these systems interact closely in regulating growth and in several cases crosstalk has been demonstrated. Importantly, these nutrient controlled systems must interact with other growth regulatory pathways.

  • 30. van der Horst, Sjors
    et al.
    Snel, Berend
    Hanson, Johannes
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC). Molecular Plant Physiology, Institute of Environmental Biology, Utrecht University, Utrecht, The Netherlands; Theoretical Biology and Bioinformatics, Department of Biology, Utrecht University, Utrecht, The Netherlands .
    Smeekens, Sjef
    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 thaliana2019In: RNA: A publication of the RNA Society, ISSN 1355-8382, E-ISSN 1469-9001, Vol. 25, no 3, p. 292-304Article in journal (Refereed)
    Abstract [en]

    Eukaryotic mRNAs contain a 5' leader sequence preceding the main open reading frame (mORF) and, depending on the species, 20%-50% of eukaryotic mRNAs harbor an upstream ORF (uORF) in the 5' leader. An unknown fraction of these uORFs encode sequence conserved peptides (conserved peptide uORFs, CPuORFs). Experimentally validated CPuORFs demonstrated to regulate the translation of downstream mORFs often do so in a metabolite concentration-dependent manner. Previous research has shown that most CPuORFs possess a start codon context suboptimal for translation initiation, which turns out to be favorable for translational regulation. The suboptimal initiation context may even include non-AUG start codons, which makes CPuORFs hard to predict. For this reason, we developed a novel pipeline to identify CPuORFs unbiased of start codon using well-annotated sequence data from 31 eudicot plant species and rice. Our new pipeline was able to identify 29 novel Arabidopsis thaliana (Arabidopsis) CPuORFs, conserved across a wide variety of eudicot species of which 15 do not initiate with an AUG start codon. In addition to CPuORFs, the pipeline was able to find 14 conserved coding regions directly upstream and in frame with the mORF, which likely initiate translation on a non-AUG start codon. Altogether, our pipeline identified highly conserved coding regions in the 5' leaders of Arabidopsis transcripts, including in genes with proven functional importance such as LHY, a key regulator of the circadian clock, and the RAPTOR1 subunit of the target of rapamycin (TOR) kinase.

  • 31. Weiste, Christoph
    et al.
    Pedrotti, Lorenzo
    Selvanayagam, Jebasingh
    Muralidhara, Prathibha
    Fröschel, Christian
    Novák, Ondřej
    Ljung, Karin
    Hanson, Johannes
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Dröge-Laser, Wolfgang
    The Arabidopsis bZIP11 transcription factor links low-energy signalling to auxin-mediated control of primary root growth2017In: PLoS Genetics, ISSN 1553-7390, E-ISSN 1553-7404, Vol. 13, no 2Article in journal (Refereed)
    Abstract [en]

    Plants have to tightly control their energy homeostasis to ensure survival and fitness under constantly changing environmental conditions. Thus, it is stringently required that energy-consuming stress-adaptation and growth-related processes are dynamically tuned according to the prevailing energy availability. The evolutionary conserved SUCROSE NON-FERMENTING1 RELATED KINASES1 (SnRK1) and the downstream group C/S1 basic leucine zipper (bZIP) transcription factors (TFs) are well-characterised central players in plants' low-energy management. Nevertheless, mechanistic insights into plant growth control under energy deprived conditions remains largely elusive. In this work, we disclose the novel function of the low-energy activated group S1 bZIP11-related TFs as regulators of auxin-mediated primary root growth. Whereas transgenic gain-of-function approaches of these bZIPs interfere with the activity of the root apical meristem and result in root growth repression, root growth of loss-of-function plants show a pronounced insensitivity to low-energy conditions. Based on ensuing molecular and biochemical analyses, we propose a mechanistic model, in which bZIP11-related TFs gain control over the root meristem by directly activating IAA3/SHY2 transcription. IAA3/SHY2 is a pivotal negative regulator of root growth, which has been demonstrated to efficiently repress transcription of major auxin transport facilitators of the PIN-FORMED (PIN) gene family, thereby restricting polar auxin transport to the root tip and in consequence auxin-driven primary root growth. Taken together, our results disclose the central low-energy activated SnRK1-C/S1-bZIP signalling module as gateway to integrate information on the plant's energy status into root meristem control, thereby balancing plant growth and cellular energy resources.

  • 32.
    Weltmeier, Fridtjof
    et al.
    Göttingen, Germany.
    Rahmani, Fatima
    Department of Molecular Plant Physiology, Utrecht University, NL-3584 CH Utrecht, The Netherlands.
    Ehlert, Andrea
    Göttingen, Germany.
    Dietrich, Katrin
    Göttingen, Germany.
    Schütze, Katia
    Tübingen, Germany.
    Wang, Xuan
    Göttingen, Germany.
    Chaban, Christina
    Tübingen, Germany.
    Hanson, Johannes
    Department of Molecular Plant Physiology, Utrecht University, NL-3584 CH Utrecht, The Netherlands.
    Teige, Markus
    University of Vienna, Vienna, Austria.
    Harter, Klaus
    Tübingen, Germany.
    Vicente-Carbajosa, Jesus
    Madrid, Spain.
    Smeekens, Sjef
    Department of Molecular Plant Physiology, Utrecht University, NL-3584 CH Utrecht, The Netherlands.
    Dröge-Laser, Wolfgang
    Göttingen, Germany.
    Expression patterns within the Arabidopsis C/S1 bZIP transcription factor network: availability of heterodimerization partners controls gene expression during stress response and development.2009In: Plant Molecular Biology, ISSN 0167-4412, E-ISSN 1573-5028, Vol. 69, no 1-2, p. 107-119Article in journal (Refereed)
    Abstract [en]

    Members of the Arabidopsis group C/S1 basic leucine zipper (bZIP) transcription factor (TF) network are proposed to implement transcriptional reprogramming of plant growth in response to energy deprivation and environmental stresses. The four group C and five group S1 members form specific heterodimers and are, therefore, considered to cooperate functionally. For example, the interplay of C/S1 bZIP TFs in regulating seed maturation genes was analyzed by expression studies and target gene regulation in both protoplasts and transgenic plants. The abundance of the heterodimerization partners significantly affects target gene transcription. Therefore, a detailed analysis of the developmental and stress related expression patterns was performed by comparing promoter: GUS and transcription data. The idea that the C/S1 network plays a role in the allocation of nutrients is supported by the defined and partially overlapping expression patterns in sink leaves, seeds and anthers. Accordingly, metabolic signals strongly affect bZIP expression on the transcriptional and/or post-transcriptional level. Sucrose induced repression of translation (SIRT) was demonstrated for all group S1 bZIPs. In particular, transcription of group S1 genes strongly responds to various abiotic stresses, such as salt (AtbZIP1) or cold (AtbZIP44). In summary, heterodimerization and expression data provide a basic framework to further determine the functional impact of the C/S1 network in regulating the plant energy balance and nutrient allocation.

  • 33. Wind, Julia J.
    et al.
    Peviani, Alessia
    Snel, Berend
    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.
    Smeekens, Sjef C.
    ABI4: versatile activator and repressor2013In: Trends in Plant Science, ISSN 1360-1385, E-ISSN 1878-4372, Vol. 18, no 3, p. 125-132Article in journal (Refereed)
    Abstract [en]

    The ABSCISIC ACID INSENSITIVE4 (ABI4) gene was discovered to be an abscisic acid (ABA) signaling responsive transcription factor active during seed germination. The evolutionary history of the ABI4 gene supports its role as an ABA signaling intermediate in land plants. Investigating the ABI4 protein-cis element interaction supports the proposal that ABI4 binding to its known CE1 cis-element competes with transcription factor binding to the overlapping G-Box element. Recent publications report on ABI4 as a regulatory factor in diverse processes. In developing seedlings, ABI4 mediates sugar signaling, lipid breakdown, and plastid-to-nucleus signaling. Moreover, ABI4 is a regulator of rosette growth, redox signaling, cell wall metabolism and the effect of nitrate on lateral root development.

  • 34.
    Wind, Julia
    et al.
    Molecular Plant Physiology, Utrecht University, Utrecht, The Netherlands.
    Smeekens, Sjef
    Molecular Plant Physiology, Utrecht University, Utrecht, The Netherlands; Centre for BioSystems Genomics, Wageningen, The Netherlands.
    Hanson, Johannes
    Molecular Plant Physiology, Utrecht University, Utrecht, The Netherlands; Centre for BioSystems Genomics, Wageningen, The Netherlands.
    Sucrose: metabolite and signaling molecule2010In: Phytochemistry, ISSN 0031-9422, E-ISSN 1873-3700, Vol. 71, no 14-15, p. 1610-1614Article in journal (Refereed)
    Abstract [en]

    Sucrose is a molecule that is synthesized only by oxygenic photosynthetic organisms. In plants, sucrose is synthesized in source tissues and then can be transported to sink tissues, where it is utilized or stored. Interestingly, sucrose is both a metabolite and a signaling molecule. Manipulating the rate of the synthesis, transport or degradation of sucrose affects plant growth, development and physiology. Altered sucrose levels changes the quantity of sucrose derived metabolites and sucrose-specific signaling. In this paper, these changes are summarized. Better understanding of sucrose metabolism and sucrose sensing systems in plants will lead to opportunities to adapt plant metabolism and growth.

  • 35. Yazdanpanah, Farzaneh
    et al.
    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. Molecular Plant Physiology, Utrecht University, Utrecht, The Netherlands..
    Hilhorst, Henk W. M.
    Bentsink, Leónie
    Differentially expressed genes during the imbibition of dormant and after-ripened seeds: a reverse genetics approach2017In: BMC Plant Biology, ISSN 1471-2229, E-ISSN 1471-2229, Vol. 17, no 1, article id 151Article in journal (Refereed)
    Abstract [en]

    BACKGROUND: Seed dormancy, defined as the incapability of a viable seed to germinate under favourable conditions, is an important trait in nature and agriculture. Despite extensive research on dormancy and germination, many questions about the molecular mechanisms controlling these traits remain unanswered, likely due to its genetic complexity and the large environmental effects which are characteristic of these quantitative traits. To boost research towards revealing mechanisms in the control of seed dormancy and germination we depend on the identification of genes controlling those traits.

    METHODS: We used transcriptome analysis combined with a reverse genetics approach to identify genes that are prominent for dormancy maintenance and germination in imbibed seeds of Arabidopsis thaliana. Comparative transcriptomics analysis was employed on freshly harvested (dormant) and after-ripened (AR; non-dormant) 24-h imbibed seeds of four different DELAY OF GERMINATION near isogenic lines (DOGNILs) and the Landsberg erecta (Ler) wild type with varying levels of primary dormancy. T-DNA knock-out lines of the identified genes were phenotypically investigated for their effect on dormancy and AR.

    RESULTS: We identified conserved sets of 46 and 25 genes which displayed higher expression in seeds of all dormant and all after-ripened DOGNILs and Ler, respectively. Knock-out mutants in these genes showed dormancy and germination related phenotypes.

    CONCLUSIONS: Most of the identified genes had not been implicated in seed dormancy or germination. This research will be useful to further decipher the molecular mechanisms by which these important ecological and commercial traits are regulated.

  • 36. Zamioudis, Christos
    et al.
    Hanson, Johannes
    Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC). Molecular Plant Physiology, Department of Biology, Faculty of Science, Utrecht University, Utrecht, the Netherlands.
    Pieterse, Corne M. J.
    beta-Glucosidase BGLU42 is a MYB72-dependent key regulator of rhizobacteria-induced systemic resistance and modulates iron deficiency responses in Arabidopsis roots2014In: New Phytologist, ISSN 0028-646X, E-ISSN 1469-8137, Vol. 204, no 2, p. 368-379Article in journal (Refereed)
    Abstract [en]

    Selected soil-borne rhizobacteria can trigger an induced systemic resistance (ISR) that is effective against a broad spectrum of pathogens. In Arabidopsis thaliana, the root-specific transcription factor MYB72 is required for the onset of ISR, but is also associated with plant survival under conditions of iron deficiency. Here, we investigated the role of MYB72 in both processes. To identify MYB72 target genes, we analyzed the root transcriptomes of wild-type Col-0, mutant myb72 and complemented 35S:FLAG-MYB72/myb72 plants in response to ISR-inducing Pseudomonas fluorescens WCS417. Five WCS417-inducible genes were misregulated in myb72 and complemented in 35S:FLAG-MYB72/myb72. Amongst these, we uncovered -glucosidase BGLU42 as a novel component of the ISR signaling pathway. Overexpression of BGLU42 resulted in constitutive disease resistance, whereas the bglu42 mutant was defective in ISR. Furthermore, we found 195 genes to be constitutively upregulated in MYB72-overexpressing roots in the absence of WCS417. Many of these encode enzymes involved in the production of iron-mobilizing phenolic metabolites under conditions of iron deficiency. We provide evidence that BGLU42 is required for their release into the rhizosphere. Together, this work highlights a thus far unidentified link between the ability of beneficial rhizobacteria to stimulate systemic immunity and mechanisms induced by iron deficiency in host plants.

  • 37. Zamioudis, Christos
    et al.
    Korteland, Jolanda
    Van Pelt, Johan A.
    van Hamersveld, Muriel
    Dombrowski, Nina
    Bai, Yang
    Hanson, Johannes
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC). Molecular Plant Physiology, Department of Biology, Faculty of Science, Utrecht University, The Netherlands.
    Van Verk, Marcel C.
    Ling, Hong-Qing
    Schulze-Lefert, Paul
    Pieterse, Corne M. J.
    Rhizobacterial volatiles and photosynthesis-related signals coordinate MYB72 expression in Arabidopsis roots during onset of induced systemic resistance and iron-deficiency responses2015In: The Plant Journal, ISSN 0960-7412, E-ISSN 1365-313X, Vol. 84, no 2, p. 309-322Article in journal (Refereed)
    Abstract [en]

    In Arabidopsis roots, the transcription factor MYB72 plays a dual role in the onset of rhizobacteria-induced systemic resistance (ISR) and plant survival under conditions of limited iron availability. Previously, it was shown that MYB72 coordinates the expression of a gene module that promotes synthesis and excretion of iron-mobilizing phenolic compounds in the rhizosphere, a process that is involved in both iron acquisition and ISR signaling. Here, we show that volatile organic compounds (VOCs) from ISR-inducing Pseudomonas bacteria are important elicitors of MYB72. In response to VOC treatment, MYB72 is co-expressed with the iron uptake-related genes FERRIC REDUCTION OXIDASE2 (FRO2) and IRON-REGULATED TRANSPORTER1 (IRT1) in a manner that is dependent on FER-LIKE IRON DEFICIENCY TRANSCRIPTION FACTOR (FIT), indicating that MYB72 is an intrinsic part of the plant's iron-acquisition response that is typically activated upon iron starvation. However, VOC-induced MYB72 expression is activated independently of iron availability in the root vicinity. Moreover, rhizobacterial VOC-mediated induction of MYB72 requires photosynthesis-related signals, while iron deficiency in the rhizosphere activates MYB72 in the absence of shoot-derived signals. Together, these results show that the ISR- and iron acquisition-related transcription factor MYB72 in Arabidopsis roots is activated by rhizobacterial volatiles and photosynthesis-related signals, and enhances the iron-acquisition capacity of roots independently of the iron availability in the rhizosphere. This work highlights the role of MYB72 in plant processes by which root microbiota simultaneously stimulate systemic immunity and activate the iron-uptake machinery in their host plants. Significance Statement Plant roots intimately interact with plant growth-promoting rhizobacteria that prime the plant immune system and aid in iron uptake two functions facilitated by the root-specific transcription factor MYB72. Here we show how MYB72 and iron uptake responses are systemically activated by photosynthesis-related signals and volatiles produced by plant growth-promoting rhizobacteria, highlighting the important role of beneficial root microbiota in supporting plant growth and health.

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