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  • 1. Ahn, Ji Hoon
    et al.
    Schmid, Markus
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology.
    Editorial overview: Growth and development: Change is in the air: how plants modulate development in response to the environment2017In: Current opinion in plant biology, ISSN 1369-5266, E-ISSN 1879-0356, Vol. 35, p. IV-VIArticle in journal (Refereed)
  • 2. Alonso, J. M.
    et al.
    Stepanova, A. N.
    Leisse, T. J.
    Kim, C. J.
    Chen, H. M.
    Shinn, P.
    Stevenson, D. K.
    Zimmerman, J.
    Barajas, P.
    Cheuk, R.
    Gadrinab, C.
    Heller, C.
    Jeske, A.
    Koesema, E.
    Meyers, C. C.
    Parker, H.
    Prednis, L.
    Ansari, Y.
    Choy, N.
    Deen, H.
    Geralt, M.
    Hazari, N.
    Hom, E.
    Karnes, M.
    Mulholland, C.
    Ndubaku, R.
    Schmidt, I.
    Guzman, P.
    Aguilar-Henonin, L.
    Schmid, M.
    Genomic Analysis Laboratory, The Salk Institute for Biological Studies, La Jolla, CA 92037, USA.
    Weigel, D.
    Carter, D. E.
    Marchand, T.
    Risseeuw, E.
    Brogden, D.
    Zeko, A.
    Crosby, W. L.
    Berry, C. C.
    Ecker, J. R.
    Genome-wide Insertional mutagenesis of Arabidopsis thaliana2003In: Science, ISSN 0036-8075, E-ISSN 1095-9203, Vol. 301, no 5633, p. 653-657Article in journal (Refereed)
  • 3.
    André, Domenique
    et al.
    Umeå Plant Science Centre, Department of Forest Genetics and Plant Physiology, Swedish University of Agricultural Sciences, Umeå, Sweden.
    Marcon, Alice
    Umeå Plant Science Centre, Department of Forest Genetics and Plant Physiology, Swedish University of Agricultural Sciences, Umeå, Sweden.
    Lee, Keh Chien
    Umeå Plant Science Centre, Department of Forest Genetics and Plant Physiology, Swedish University of Agricultural Sciences, Umeå, Sweden.
    Goretti, Daniela
    Umeå Plant Science Centre, Department of Forest Genetics and Plant Physiology, Swedish University of Agricultural Sciences, Umeå, Sweden.
    Zhang, Bo
    Umeå Plant Science Centre, Department of Forest Genetics and Plant Physiology, Swedish University of Agricultural Sciences, Umeå, Sweden.
    Delhomme, Nicolas
    Umeå Plant Science Centre, Department of Forest Genetics and Plant Physiology, Swedish University of Agricultural Sciences, Umeå, Sweden.
    Schmid, Markus
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Nilsson, Ove
    Umeå Plant Science Centre, Department of Forest Genetics and Plant Physiology, Swedish University of Agricultural Sciences, Umeå, Sweden.
    FLOWERING LOCUS T paralogs control the annual growth cycle in Populus trees2022In: Current Biology, ISSN 0960-9822, E-ISSN 1879-0445, Vol. 32, no 13, p. 2988-2996.e4Article in journal (Refereed)
    Abstract [en]

    In temperate and boreal regions, perennials adapt their annual growth cycle to the change of seasons. These adaptations ensure survival in harsh environmental conditions, allowing growth at different latitudes and altitudes, and are therefore tightly regulated. Populus tree species cease growth and form terminal buds in autumn when photoperiod falls below a certain threshold.1 This is followed by establishment of dormancy and cold hardiness over the winter. At the center of the photoperiodic pathway in Populus is the gene FLOWERING LOCUS T2 (FT2), which is expressed during summer and harbors significant SNPs in its locus associated with timing of bud set.1–4 The paralogous gene FT1, on the other hand, is hyper-induced in chilling buds during winter.3,5 Even though its function is so far unknown, it has been suggested to be involved in the regulation of flowering and the release of winter dormancy.3,5 In this study, we employ CRISPR-Cas9-mediated gene editing to individually study the function of the FT-like genes in Populus trees. We show that while FT2 is required for vegetative growth during spring and summer and regulates the entry into dormancy, expression of FT1 is absolutely required for bud flush in spring. Gene expression profiling suggests that this function of FT1 is linked to the release of winter dormancy rather than to the regulation of bud flush per se. These data show how FT duplication and sub-functionalization have allowed Populus trees to regulate two completely different and major developmental control points during the yearly growth cycle.

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  • 4.
    Benstein, Ruben M.
    et al.
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Schmid, Markus
    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 Plant Biology, Linnean Centre for Plant Biology, Swedish University of Agricultural Sciences, Uppsala, Sweden.
    You, Yuan
    Center for Plant Molecular Biology (ZMBP), Department of General Genetics, Eberhard Karls University of Tübingen, Tübingen, Germany; Department of Molecular Life Sciences, Technical University of Munich, Freising, Germany.
    Isolation of nuclei tagged in specific cell types (INTACT) in Arabidopsis2023In: Flower development: methods and protocols / [ed] José Luis Riechmann; Cristina Ferrándiz, New york: Humana Press, 2023, 2, Vol. 2686, p. 313-328Chapter in book (Refereed)
    Abstract [en]

    Many functionally distinct plant tissues have relatively low numbers of cells that are embedded within complex tissues. For example, the shoot apical meristem (SAM) consists of a small population of pluripotent stem cells surrounded by developing leaves and/or flowers at the growing tip of the plant. It is technically challenging to collect enough high-quality SAM samples for molecular analyses. Isolation of Nuclei Tagged in specific Cell Types (INTACT) is an easily reproducible method that allows the enrichment of biotin-tagged cell-type-specific nuclei from the total nuclei pool using biotin-streptavidin affinity purification. Here, we provide a detailed INTACT protocol for isolating nuclei from the Arabidopsis SAM. One can also adapt this protocol to isolate nuclei from other tissues and cell types for investigating tissue/cell-type-specific transcriptome and epigenome and their changes during developmental programs at a high spatiotemporal resolution. Furthermore, due to its low cost and simple procedures, INTACT can be conducted in any standard molecular laboratory.

  • 5. Brandt, Ronny
    et al.
    Salla-Martret, Merce
    Bou-Torrent, Jordi
    Musielak, Thomas
    Stahl, Mark
    Lanz, Christa
    Ott, Felix
    Schmid, Markus
    Department of Molecular Biology, Max Planck Institute for Developmental Biology, 72076 Tübingen, Germany.
    Greb, Thomas
    Schwarz, Martina
    Choi, Sang-Bong
    Barton, M. Kathryn
    Reinhart, Brenda J.
    Liu, Tie
    Quint, Marcel
    Palauqui, Jean-Christophe
    Martinez-Garcia, Jaime F.
    Wenkel, Stephan
    Genome-wide binding-site analysis of REVOLUTA reveals a link between leaf patterning and light-mediated growth responses2012In: The Plant Journal, ISSN 0960-7412, E-ISSN 1365-313X, Vol. 72, no 1, p. 31-42Article in journal (Refereed)
  • 6.
    Brunoni, Federica
    et al.
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC). Umeå Plant Science Centre, Department of Forest Genetics and PlantPhysiology, Swedish University of Agricultural Sciences (SLU), 90183, Umeå, Sweden.
    Collani, Silvio
    Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC). Umeå University, Faculty of Science and Technology, Department of Plant Physiology.
    Casanova-Saez, Ruben
    Simura, Jan
    Karady, Michal
    Schmid, Markus
    Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC). Umeå University, Faculty of Science and Technology, Department of Plant Physiology.
    Ljung, Karin
    Bellini, C
    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, INRAE, AgroParisTech, Université Paris-Saclay, 78000, Versailles, France.
    Conifers exhibit a characteristic inactivation of auxin to maintain tissue homeostasis2020In: New Phytologist, ISSN 0028-646X, E-ISSN 1469-8137, Vol. 226, no 6, p. 1753-1765Article in journal (Refereed)
    Abstract [en]

    Dynamic regulation of the concentration of the natural auxin (IAA) is essential to coordinate most of the physiological and developmental processes and responses to environmental changes. Oxidation of IAA is a major pathway to control auxin concentrations in angiosperms and, along with IAA conjugation, to respond to perturbation of IAA homeostasis. However, these regulatory mechanisms remain poorly investigated in conifers. To reduce this knowledge gap, we investigated the different contributions of the IAA inactivation pathways in conifers. MS-based quantification of IAA metabolites under steady-state conditions and after perturbation was investigated to evaluate IAA homeostasis in conifers. Putative Picea abies GH3 genes (PaGH3) were identified based on a comprehensive phylogenetic analysis including angiosperms and basal land plants. Auxin-inducible PaGH3 genes were identified by expression analysis and their IAA-conjugating activity was explored. Compared to Arabidopsis, oxidative and conjugative pathways differentially contribute to reduce IAA concentrations in conifers. We demonstrated that the oxidation pathway plays a marginal role in controlling IAA homeostasis in spruce. By contrast, an excess of IAA rapidly activates GH3-mediated irreversible conjugation pathways. Taken together, these data indicate that a diversification of IAA inactivation mechanisms evolved specifically in conifers.

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  • 7.
    Brunoni, Federica
    et al.
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC). Umeå Plant Science Centre, Department of Forest Genetics and Plant Physiology, Swedish University of Agricultural Sciences (SLU), Umeå, Sweden; Present address: Laboratory of Growth Regulators, Faculty of Science, Palacký University & Institute of Experimental Botany, The Czech Academy of Sciences, Šlechtitelů 27, 78371 Olomouc, Czech Republic.
    Collani, Silvio
    Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC). Umeå University, Faculty of Science and Technology, Department of Plant Physiology.
    Simura, Jan
    Schmid, Markus
    Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC). Umeå University, Faculty of Science and Technology, Department of Plant Physiology.
    Bellini, Catherine
    Ljung, Karin
    A bacterial assay for rapid screening of IAA catabolic enzymes2019In: Plant Methods, E-ISSN 1746-4811, Vol. 15, no 1, article id 126Article in journal (Refereed)
    Abstract [en]

    Background: Plants rely on concentration gradients of the native auxin, indole-3-acetic acid (IAA), to modulate plant growth and development. Both metabolic and transport processes participate in the dynamic regulation of IAA homeostasis. Free IAA levels can be reduced by inactivation mechanisms, such as conjugation and degradation. IAA can be conjugated via ester linkage to glucose, or via amide linkage to amino acids, and degraded via oxidation. Members of the UDP glucosyl transferase (UGT) family catalyze the conversion of IAA to indole-3-acetyl-1-glucosyl ester (IAGlc); by contrast, IAA is irreversibly converted to indole-3-acetyl-L-aspartic acid (IAAsp) and indole-3-acetyl glutamic acid (IAGlu) by Group II of the GRETCHEN HAGEN3 (GH3) family of acyl amido synthetases. Dioxygenase for auxin oxidation (DAO) irreversibly oxidizes IAA to oxindole-3-acetic acid (oxIAA) and, in turn, oxIAA can be further glucosylated to oxindole-3-acetyl-1-glucosyl ester (oxIAGlc) by UGTs. These metabolic pathways have been identified based on mutant analyses, in vitro activity measurements, and in planta feeding assays. In vitro assays for studying protein activity are based on producing Arabidopsis enzymes in a recombinant form in bacteria or yeast followed by recombinant protein purification. However, the need to extract and purify the recombinant proteins represents a major obstacle when performing in vitro assays.

    Results: In this work we report a rapid, reproducible and cheap method to screen the enzymatic activity of recombinant proteins that are known to inactivate IAA. The enzymatic reactions are carried out directly in bacteria that produce the recombinant protein. The enzymatic products can be measured by direct injection of a small supernatant fraction from the bacterial culture on ultrahigh-performance liquid chromatography coupled to electrospray ionization tandem spectrometry (UHPLC–ESI-MS/MS). Experimental procedures were optimized for testing the activity of different classes of IAA-modifying enzymes without the need to purify recombinant protein.

    Conclusions: This new method represents an alternative to existing in vitro assays. It can be applied to the analysis of IAA metabolites that are produced upon supplementation of substrate to engineered bacterial cultures and can be used for a rapid screening of orthologous candidate genes from non-model species.

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  • 8. Capovilla, Giovanna
    et al.
    Delhomme, Nicolas
    Collani, Silvio
    Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC). Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Max Planck Institute for Developmental Biology, Department of Molecular Biology, Tübingen, Germany.
    Shutava, Iryna
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Bezrukov, Ilja
    Symeonidi, Efthymia
    Amorim, Marcella de Francisco
    Laubinger, Sascha
    Schmid, Markus
    Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC). Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Max Planck Institute for Developmental Biology, Department of Molecular Biology, Tübingen, Germany.
    PORCUPINE regulates development in response to temperature through alternative splicing2018In: Nature plants, ISSN 2055-026X, Vol. 4, no 8, p. 534-539Article in journal (Refereed)
    Abstract [en]

    Recent findings suggest that alternative splicing has a critical role in controlling the responses of plants to temperature variations. However, alternative splicing factors in plants are largely uncharacterized. Here we establish the putative splice regulator, PORCUPINE (PCP), as temperature-specific regulator of development in Arabidopsis thaliana. Our findings point to the misregulation of WUSCHEL and CLAVATA3 as the possible cause for the meristem defects affecting the pcp-1 loss-of-function mutants at low temperatures.

  • 9. Capovilla, Giovanna
    et al.
    Pajoro, Alice
    Immink, Richard GH
    Schmid, Markus
    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 Biology, Max Planck Institute for Developmental Biology, 72074 Tübingen, Germany.
    Role of alternative pre-mRNA splicing in temperature signaling2015In: Current opinion in plant biology, ISSN 1369-5266, E-ISSN 1879-0356, Vol. 27, p. 97-103Article, review/survey (Refereed)
    Abstract [en]

    Developmental plasticity enables plants to respond rapidly to changing environmental conditions, such as temperature fluctuations. Understanding how plants measure temperature and integrate this information into developmental programs at the molecular level will be essential to breed thermo-tolerant crop varieties. Recent studies identified alternative splicing (AS) as a possible 'molecular thermometer', allowing plants to quickly adjust the abundance of functional transcripts to environmental perturbations. In this review, recent advances regarding the effects of temperature-responsive AS on plant development will be discussed, with emphasis on the circadian clock and flowering time control. The challenge for the near future will be to understand the molecular mechanisms by which temperature can influence AS regulation.

  • 10. Capovilla, Giovanna
    et al.
    Schmid, Markus
    Max Planck Institute for Developmental Biology, Department of Molecular Biology, Tübingen, Germany.
    Posé, David
    Control of flowering by ambient temperature2015In: Journal of Experimental Botany, ISSN 0022-0957, E-ISSN 1460-2431, Vol. 66, no 1, p. 59-69Article in journal (Refereed)
    Abstract [en]

    The timing of flowering is a crucial decision in the life cycle of plants since favourable conditions are needed to maximize reproductive success and, hence, the survival of the species. It is therefore not surprising that plants constantly monitor endogenous and environmental signals, such as day length (photoperiod) and temperature, to adjust the timing of the floral transition. Temperature in particular has been shown to have a tremendous effect on the timing of flowering: the effect of prolonged periods of cold, called the vernalization response, has been extensively studied and the underlying epigenetic mechanisms are reasonably well understood in Arabidopsis thaliana. In contrast, the effect of moderate changes in ambient growth temperature on the progression of flowering, the thermosensory pathway, is only starting to be understood on the molecular level. Several genes and molecular mechanisms underlying the thermosensory pathway have already been identified and characterized in detail. At a time when global temperature is rising due to climate change, this knowledge will be pivotal to ensure crop production in the future.

  • 11. Capovilla, Giovanna
    et al.
    Symeonidi, Efthymia
    Wu, Rui
    Schmid, Markus
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC). Max Planck Institute for Developmental Biology, Department of Molecular Biology, Spemannstr. 35, 72076 Tübingen, Germany.
    Contribution of major FLM isoforms to temperature-dependent flowering in Arabidopsis thaliana2017In: Journal of Experimental Botany, ISSN 0022-0957, E-ISSN 1460-2431, Vol. 68, no 18, p. 5117-5127Article in journal (Refereed)
    Abstract [en]

    FLOWERING LOCUS M (FLM), a component of the thermosensory flowering time pathway in Arabidopsis thaliana, is regulated by temperature-dependent alternative splicing (AS). The main splicing variant, FLM-beta, is a well-documented floral repressor that is down-regulated in response to increasing ambient growth temperature. Two hypotheses have been formulated to explain how flowering time is modulated by AS of FLM. In the first model a second splice variant, FLM-delta, acts as a dominant negative isoform that competes with FLM-beta at elevated ambient temperatures, thereby indirectly promoting flowering. Alternatively, it has been suggested that the induction of flowering at elevated temperatures is caused only by reduced FLM-beta expression. To better understand the role of the two FLM splice forms, we employed CRISPR/Cas9 technology to specifically delete the exons that characterize each splice variant. Lines that produced repressive FLM-beta but were incapable of producing FLM-delta were late flowering. In contrast, FLM-beta knockout lines that still produced FLM-delta flowered early, but not earlier than the flm-3 loss of function mutant, as would be expected if FLM-delta had a dominant-negative effect on flowering. Our data support the role of FLM-beta as a flower repressor and provide evidence that a contribution of FLM-delta to the regulation of flowering time in wild-type A. thaliana seems unlikely.

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  • 12.
    Collani, Silvio
    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. Max Planck Institute for Developmental Biology,Department of Molecular Biology, Tübingen, Germany.
    Neumann, Manuela
    Yant, Levi
    Schmid, Markus
    Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC). Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Max Planck Institute for Developmental Biology,Department of Molecular Biology, Tübingen, Germany; Beijing Advanced Innovation Centre for Tree Breeding by Molecular Design, Beijing Forestry University, Beijing, People’s Republic of China.
    FT Modulates Genome-Wide DNA-Binding of the bZIP Transcription Factor FD2019In: Plant Physiology, ISSN 0032-0889, E-ISSN 1532-2548, Vol. 180, no 1, p. 367-380Article in journal (Refereed)
    Abstract [en]

    The transition to flowering is a crucial step in the plant life cycle that is controlled by multiple endogenous and environmental cues, including hormones, sugars, temperature, and photoperiod. Permissive photoperiod induces the expression of FLOWERING LOCUS T (FT) in the phloem companion cells of leaves. The FT protein then acts as a florigen that is transported to the shoot apical meristem, where it physically interacts with the Basic Leucine Zipper Domain transcription factor FD and 14-3-3 proteins. However, despite the importance of FD in promoting flowering, its direct transcriptional targets are largely unknown. Here, we combined chromatin immunoprecipitation sequencing and RNA sequencing to identify targets of FD at the genome scale and assessed the contribution of FT to DNA binding. We further investigated the ability of FD to form protein complexes with FT and TERMINAL FLOWER1 through interaction with 14-3-3 proteins. Importantly, we observed direct binding of FD to targets involved in several aspects of plant development. These target genes were previously unknown to be directly related to the regulation of flowering time. Our results confirm FD as a central regulator of floral transition at the shoot meristem and provide evidence for crosstalk between the regulation of flowering and other signaling pathways, such as pathways involved in hormone signaling.

  • 13. Conn, Vanessa M.
    et al.
    Hugouvieux, Veronique
    Nayak, Aditya
    Conos, Stephanie A.
    Capovilla, Giovanna
    Cildir, Gokhan
    Jourdain, Agnes
    Tergaonkar, Vinay
    Schmid, Markus
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Zubieta, Chloe
    Conn, Simon J.
    A circRNA from SEPALLATA3 regulates splicing of its cognate mRNA through R-loop formation2017In: Nature Plants, ISSN 2055-026X, Vol. 3, no 5, article id 17053Article in journal (Refereed)
    Abstract [en]

    Circular RNAs (circRNAs) are a diverse and abundant class of hyper-stable, non-canonical RNAs that arise through a form of alternative splicing (AS) called back-splicing. These single-stranded, covalently-closed circRNA molecules have been identified in all eukaryotic kingdoms of life(1), yet their functions have remained elusive. Here, we report that circRNAs can be used as bona fide biomarkers of functional, exon-skipped AS variants in Arabidopsis, including in the homeotic MADS-box transcription factor family. Furthermore, we demonstrate that circRNAs derived from exon 6 of the SEPALLATA3 (SEP3) gene increase abundance of the cognate exon-skipped AS variant (SEP3.3 which lacks exon 6), in turn driving floral homeotic phenotypes. Toward demonstrating the underlying mechanism, we show that the SEP3 exon 6 circRNA can bind strongly to its cognate DNA locus, forming an RNA: DNA hybrid, or R-loop, whereas the linear RNA equivalent bound significantly more weakly to DNA. R-loop formation results in transcriptional pausing, which has been shown to coincide with splicing factor recruitment and AS(2-4). This report presents a novel mechanistic insight for how at least a subset of circRNAs probably contribute to increased splicing efficiency of their cognate exon-skipped messenger RNA and provides the first evidence of an organismal-level phenotype mediated by circRNA manipulation.

  • 14.
    Dikaya, Varvara
    et al.
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    El Arbi, Nabila
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Rojas-Murcia, Nelson
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Muniz Nardeli, Sarah
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Goretti, Daniela
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Schmid, Markus
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC). Beijing Advanced Innovation Centre for Tree Breeding by Molecular Design, Beijing Forestry University, Beijing, China.
    Insights into the role of alternative splicing in plant temperature response2021In: Journal of Experimental Botany, ISSN 0022-0957, E-ISSN 1460-2431, Vol. 72, no 21, p. 7384-7403Article, review/survey (Refereed)
    Abstract [en]

    Alternative splicing occurs in all eukaryotic organisms. Since the first description of multiexon genes and the splicing machinery, the field has expanded rapidly, especially in animals and yeast. However, our knowledge about splicing in plants is still quite fragmented. Though eukaryotes show some similarity in the composition and dynamics of their splicing machinery, observations of unique plant traits are only starting to emerge. For instance, plant alternative splicing is closely linked to their ability to perceive various environmental stimuli. Due to their sessile lifestyle, temperature is a central source of information, allowing plants to adjust their development to match current growth conditions. Hence, seasonal temperature fluctuations and day-night cycles can strongly influence plant morphology across developmental stages. Here we discuss available data on temperature-dependent alternative splicing in plants. Given its fragmented state, it is not always possible to fit specific observations into a coherent picture, yet it is sufficient to estimate the complexity of this field and the need for further research. Better understanding of alternative splicing as a part of plant temperature response and adaptation may also prove to be a powerful tool for both fundamental and applied sciences.

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  • 15. Dinh, Thanh Theresa
    et al.
    Girke, Thomas
    Liu, Xigang
    Yant, Levi
    Schmid, Markus
    Max Planck Institute for Developmental Biology, Department of Molecular Biology, Tuebingen, Germany.
    Chen, Xuemei
    The floral homeotic protein APETALA2 recognizes and acts through an AT-rich sequence element2012In: Development, ISSN 0950-1991, E-ISSN 1477-9129, Vol. 139, no 11, p. 1978-1986Article in journal (Refereed)
  • 16. Dohmann, Esther M. N.
    et al.
    Levesque, Mitchell P.
    De Veylder, Lieven
    Reichardt, Ilka
    Juergens, Gerd
    Schmid, Markus
    Tübingen University, Center for Plant Molecular Biology, Department of Developmental Genetics, Auf der Morgenstelle 3-5, 72076 Tübingen, Germany.
    Schwechheimer, Claus
    The Arabidopsis COP9 signalosome is essential for G2 phase progression and genomic stability2008In: Development, ISSN 0950-1991, E-ISSN 1477-9129, Vol. 135, no 11, p. 2013-2022Article in journal (Refereed)
  • 17. Engelhorn, Julia
    et al.
    Blanvillain, Robert
    Kroner, Christian
    Parrinello, Hugues
    Rohmer, Marine
    Pose, David
    Ott, Felix
    Schmid, Markus
    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 Biology, Max Planck Institute for Developmental Biology, Tübingen, Germany.
    Carles, Cristel C.
    Dynamics of H3K4me3 Chromatin Marks Prevails over H3K27me3 for Gene Regulation during Flower Morphogenesis in Arabidopsis thaliana2017In: Epigenomes, ISSN 2075-4655, Vol. 1, no 2, article id 8Article in journal (Refereed)
    Abstract [en]

    Plant life-long organogenesis involves sequential, time and tissue specific expression of developmental genes. This requires activities of Polycomb Group (PcG) and trithorax Group complexes (trxG), respectively responsible for repressive Histone 3 trimethylation at lysine 27 (H3K27me3) and activation-related Histone 3 trimethylation at lysine 4 (H3K4me3). However, the genome-wide dynamics in histone modifications that occur during developmental processes have remained elusive. Here, we report the distributions of H3K27me3 and H3K4me3 along with expression changes, in a developmental series including Arabidopsis thaliana leaf and three stages of flower development. We found that chromatin mark levels are highly dynamic over the time series on nearly half of all Arabidopsis genes. Moreover, during early flower morphogenesis, changes in H3K4me3 prevail over changes in H3K27me3 and quantitatively correlate with expression changes, while H3K27me3 changes occur later. Notably, we found that H3K4me3 increase during the early activation of PcG target genes while H3K27me3 level remain relatively constant at the locus. Our results reveal that H3K4me3 predicts changes in gene expression better than H3K27me3, unveil unexpected chromatin mechanisms at gene activation and underline the relevance of tissue-specific temporal epigenomics.

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  • 18. Galvao, Vinicius C.
    et al.
    Horrer, Daniel
    Kuettner, Frank
    Schmid, Markus
    Max Planck Institute for Developmental Biology, Department of Molecular Biology, Tuebingen, Germany.
    Spatial control of flowering by DELLA proteins in Arabidopsis thaliana2012In: Development, ISSN 0950-1991, E-ISSN 1477-9129, Vol. 139, no 21, p. 4072-4082Article in journal (Refereed)
  • 19. Galvao, Vinicius C.
    et al.
    Nordstroem, Karl J. V.
    Lanz, Christa
    Sulz, Patric
    Mathieu, Johannes
    Pose, David
    Schmid, Markus
    Max Planck Institute for Developmental Biology, Department of Molecular Biology, Tuebingen, Germany.
    Weigel, Detlef
    Schneeberger, Korbinian
    Synteny-based mapping-by-sequencing enabled by targeted enrichment2012In: The Plant Journal, ISSN 0960-7412, E-ISSN 1365-313X, Vol. 71, no 3, p. 517-526Article in journal (Refereed)
  • 20. Galvao, Vinicius Costa
    et al.
    Collani, Silvio
    Horrer, Daniel
    Schmid, Markus
    Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Gibberellic acid signaling is required for ambient temperature-mediated induction of flowering in Arabidopsis thaliana2015In: The Plant Journal, ISSN 0960-7412, E-ISSN 1365-313X, Vol. 84, no 5, p. 949-962Article in journal (Refereed)
    Abstract [en]

    Distinct molecular mechanisms integrate changes in ambient temperature into the genetic pathways that govern flowering time in Arabidopsis thaliana. Temperature-dependent eviction of the histone variant H2A.Z from nucleosomes has been suggested to facilitate the expression of FT by PIF4 at elevated ambient temperatures. Here we show that, in addition to PIF4, PIF3 and PIF5, but not PIF1 and PIF6, can promote flowering when expressed specifically in phloem companion cells (PCC), where they can induce FT and its close paralog, TSF. However, despite their strong potential to promote flowering, genetic analyses suggest that the PIF genes seem to have only a minor role in adjusting flowering in response to photoperiod or high ambient temperature. In addition, loss of PIF function only partially suppressed the early flowering phenotype and FT expression of the arp6 mutant, which is defective in H2A.Z deposition. In contrast, the chemical inhibition of gibberellic acid (GA) biosynthesis resulted in a strong attenuation of early flowering and FT expression in arp6. Furthermore, GA was able to induce flowering at low temperature (15 degrees C) independently of FT, TSF, and the PIF genes, probably directly at the shoot apical meristem. Together, our results suggest that the timing of the floral transition in response to ambient temperature is more complex than previously thought and that GA signaling might play a crucial role in this process.

  • 21. Galvao, Vinicius Costa
    et al.
    Schmid, Markus
    Max Planck Institute for Developmental Biology, Department of Molecular Biology, Spemannstrasse 35, 72076 Tübingen, Germany.
    Regulation of Flowering by Endogenous Signals2014In: Molecular Genetics of Floral Transition and Flower Development, 2014Chapter in book (Refereed)
  • 22. Gietl, C.
    et al.
    Schmid, M.
    Lehrstuhl für Botanik, Biologikum-Weihenstephan, Technische Universität München, Am Hochanger 4, 85350 Freising, Germany.
    Ricinosomes: an organelle for developmentally regulated programmed cell death in senescing plant tissues2001In: Die Naturwissenschaften, ISSN 0028-1042, E-ISSN 1432-1904, Vol. 88, no 2, p. 49-58Article in journal (Refereed)
  • 23.
    Goretti, Daniela
    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.
    Silvestre, Marina
    Collani, Silvio
    Langenecker, Tobias
    Mendez, Carla
    Madueno, Francisco
    Schmid, Markus
    Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC). Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Beijing Advanced Innovation Centre for Tree Breedingby Molecular Design, Beijing Forestry University, Beijing, People’s Republic of China.
    TERMINAL FLOWER1 Functions as a Mobile Transcriptional Cofactor in the Shoot Apical Meristem2020In: Plant Physiology, ISSN 0032-0889, E-ISSN 1532-2548, Vol. 182, no 4, p. 2081-2095Article in journal (Refereed)
    Abstract [en]

    TERMINAL FLOWER1 acts in the shoot apical meristem as a mobile cell-non-autonomous transcriptional cofactor that associates with DNA to regulate meristem indeterminacy and flowering. The floral transition is a critical step in the life cycle of flowering plants, and several mechanisms control this finely orchestrated process. TERMINAL FLOWER1 (TFL1) is a floral repressor and close relative of the florigen, FLOWERING LOCUS T (FT). During the floral transition, TFL1 expression is up-regulated in the inflorescence apex to maintain the indeterminate growth of the shoot apical meristem (SAM). Both TFL1 and FT are mobile proteins, but they move in different ways. FT moves from the leaves to the SAM, while TFL1 appears to move within the SAM. The importance of TFL1 movement for its function in the regulation of flowering time and shoot indeterminacy and its molecular function are still largely unclear. Our results using Arabidopsis (Arabidopsis thaliana) indicate that TFL1 moves from its place of expression in the center of the SAM to the meristem layer L1 and that the movement in the SAM is required for the regulation of the floral transition. Chromatin immunoprecipitation sequencing and RNA sequencing demonstrated that TFL1 functions as a cotranscription factor that associates with and regulates the expression of hundreds of genes. These newly identified direct TFL1 targets provide the possibility to discover new roles for TFL1 in the regulation of floral transition and inflorescence development.

  • 24. Helm, Michael
    et al.
    Schmid, Markus
    Technische Universität München, Lehrstuhl für Botanik, Biologikum-Weihenstephan, Am Hochanger 4, D-85350 Freising, Germany.
    Hierl, Georg
    Terneus, Kimberly
    Tan, Li
    Lottspeich, Friedrich
    Kieliszewski, Marcia J.
    Gietl, Christine
    KDEL-tailed cysteine endopeptidases involved in programmed cell death, intercalation of new cells, and dismantling of extensin scaffolds2008In: American Journal of Botany, ISSN 0002-9122, E-ISSN 1537-2197, Vol. 95, no 9, p. 1049-1062Article in journal (Refereed)
  • 25. Henz, Stefan R.
    et al.
    Cumbie, Jason S.
    Kasschau, Kristin D.
    Lohmann, Jan U.
    Carrington, James C.
    Weigel, Detlef
    Schmid, Markus
    Max Planck Institute for Developmental Biology, Department of Molecular Biology, Tuebingen, Germany.
    Distinct expression patterns of natural antisense transcripts in arabidopsis2007In: Plant Physiology, ISSN 0032-0889, E-ISSN 1532-2548, Vol. 144, no 3, p. 1247-1255Article in journal (Refereed)
  • 26. Huijser, Peter
    et al.
    Schmid, Markus
    Max Planck Institute for Plant Breeding Research, Carl-von-Linné-Weg 10, 50829 Cologne, Germany.
    The control of developmental phase transitions in plants2011In: Development, ISSN 0950-1991, E-ISSN 1477-9129, Vol. 138, no 19, p. 4117-4129Article in journal (Refereed)
  • 27. Immink, Richard G. H.
    et al.
    Pose, David
    Ferrario, Silvia
    Ott, Felix
    Kaufmann, Kerstin
    Valentim, Felipe Leal
    de Folter, Stefan
    van der Wal, Froukje
    van Dijk, Aalt D. J.
    Schmid, Markus
    Max Planck Institute for Developmental Biology, Department of Molecular Biology, Tuebingen, Germany.
    Angenent, Gerco C.
    Characterization of SOC1's Central Role in Flowering by the Identification of Its Upstream and Downstream Regulators2012In: Plant Physiology, ISSN 0032-0889, E-ISSN 1532-2548, Vol. 160, no 1, p. 433-449Article in journal (Refereed)
  • 28. Koo, Sung C.
    et al.
    Bracko, Oliver
    Park, Mi S.
    Schwab, Rebecca
    Chun, Hyun J.
    Park, Kyoung M.
    Seo, Jun S.
    Grbic, Vojislava
    Balasubramanian, Sureshkumar
    Schmid, Markus
    Department of Molecular Biology, Max Planck Institute for Developmental Biology, D-72076 Tübingen, Germany.
    Godard, Francois
    Yun, Dae-Jin
    Lee, Sang Y.
    Cho, Moo J.
    Weigel, Detlef
    Kim, Min C.
    Control of lateral organ development and flowering time by the Arabidopsis thaliana MADS-box Gene AGAMOUS-LIKE62010In: The Plant Journal, ISSN 0960-7412, E-ISSN 1365-313X, Vol. 62, no 5, p. 807-816Article in journal (Refereed)
  • 29. Lee, Jeong Hwan
    et al.
    Ryu, Hak-Seung
    Chung, Kyung Sook
    Pose, David
    Kim, Soonkap
    Schmid, Markus
    Max Planck Institute for Developmental Biology, Department of Molecular Biology, Spemannstrasse 35, 72076 Tübingen, Germany.
    Ahn, Ji Hoon
    Regulation of Temperature-Responsive Flowering by MADS-Box Transcription Factor Repressors2013In: Science, ISSN 0036-8075, E-ISSN 1095-9203, Vol. 342, no 6158, p. 628-632Article in journal (Refereed)
  • 30.
    Lee, Joanne E.
    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.
    Goretti, Daniela
    Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC). Umeå University, Faculty of Science and Technology, Department of Plant Physiology.
    Neumann, Manuela
    Department of Molecular Biology, Max Planck Institute for Developmental Biology, Tübingen 72076, Germany.
    Schmid, Markus
    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 Biology, Max Planck Institute for Developmental Biology, Germany; Beijing Advanced Innovation Centre for Tree Breeding by Molecular Design, Beijing Forestry University, People’s Republic of China.
    You, Yuan
    Department of Molecular Biology, Max Planck Institute for Developmental Biology, Tübingen 72076, Germany; Center for Plant Molecular Biology (ZMBP), Department of General Genetics, University Tübingen, Tübingen 72076, Germany.
    A gibberellin methyltransferase modulates the timing of floral transition at the Arabidopsis shoot meristem2020In: Physiologia Plantarum, ISSN 0031-9317, E-ISSN 1399-3054, Vol. 170, no 4, p. 474-487Article in journal (Refereed)
    Abstract [en]

    The transition from vegetative to reproductive growth is a key event in the plant life cycle. Plants therefore use a variety of environmental and endogenous signals to determine the optimal time for flowering to ensure reproductive success. These signals are integrated at the shoot apical meristem (SAM), which subsequently undergoes a shift in identity and begins producing flowers rather than leaves, while still maintaining pluripotency and meristematic function. Gibberellic acid (GA), an important hormone associated with cell growth and differentiation, has been shown to promote flowering in many plant species including Arabidopsis thaliana , but the details of how spatial and temporal regulation of GAs in the SAM contribute to floral transition are poorly understood. In this study, we show that the gene GIBBERELLIC ACID METHYLTRANSFERASE 2 (GAMT2 ), which encodes a GA‐inactivating enzyme, is significantly upregulated at the SAM during floral transition and contributes to the regulation of flowering time. Loss of GAMT2 function leads to early flowering, whereas transgenic misexpression of GAMT2 in specific regions around the SAM delays flowering. We also found that GAMT2 expression is independent of the key floral regulator LEAFY but is strongly increased by the application of exogenous GA. Our results indicate that GAMT2 is a repressor of flowering that may act as a buffer of GA levels at the SAM to help prevent premature flowering.

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  • 31.
    Lee, Joanne E.
    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.
    Neumann, Manuela
    Duro, Daniel Iglesias
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Schmid, Markus
    Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC). Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Max Planck Institute for Developmental Biology, Department of Molecular Biology, Tu ¨bingen, Germany; Beijing Advanced Innovation Centre for Tree Breeding by Molecular Design, Beijing Forestry University, Beijing, People's Republic of China.
    CRISPR-based tools for targeted transcriptional and epigenetic regulation in plants2019In: PLOS ONE, E-ISSN 1932-6203, Vol. 14, no 9, article id e0222778Article in journal (Refereed)
    Abstract [en]

    Programmable gene regulators that can modulate the activity of selected targets in trans are a useful tool for probing and manipulating gene function. CRISPR technology provides a convenient method for gene targeting that can also be adapted for multiplexing and other modifications to enable strong regulation by a range of different effectors. We generated a vector toolbox for CRISPR/dCas9-based targeted gene regulation in plants, modified with the previously described MS2 system to amplify the strength of regulation, and using Golden Gate-based cloning to enable rapid vector assembly with a high degree of flexibility in the choice of promoters, effectors and targets. We tested the system using the floral regulator FLOWERING LOCUS T (FT) as a target and a range of different effector domains including the transcriptional activator VP64, the H3K27 acetyltransferase p300 and the H3K9 methyltransferase KRYPTONITE. When transformed into Arabidopsis thaliana, several of the constructs caused altered flowering time phenotypes that were associated with changes in FT expression and/or epigenetic status, thus demonstrating the effectiveness of the system. The MS2-CRISPR/dCas9 system can be used to modulate transcriptional activity and epigenetic status of specific target genes in plants, and provides a versatile tool that can easily be used with different targets and types of regulation for a range of applications.

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  • 32. Lempe, J.
    et al.
    Balasubramanian, S.
    Sureshkumar, S.
    Singh, A.
    Schmid, M.
    Department of Molecular Biology, Max Planck Institute for Developmental Biology, Tübingen, Germany .
    Weigel, D.
    Diversity of flowering responses in wild Arabidopsis thaliana strains2005In: PLOS Genetics, ISSN 1553-7390, E-ISSN 1553-7404, Vol. 1, no 1, p. 109-118Article in journal (Refereed)
  • 33. Lutz, Ulrich
    et al.
    Posé, David
    Pfeifer, Matthias
    Gundlach, Heidrun
    Hagmann, Jörg
    Wang, Congmao
    Weigel, Detlef
    Mayer, Klaus F. X.
    Schmid, Markus
    Max Planck Institute for Developmental Biology, Department of Molecular Biology, Spemannstrasse 35, 72076 Tübingen, Germany.
    Schwechheimer, Claus
    Modulation of Ambient Temperature-Dependent Flowering in Arabidopsis thaliana by Natural Variation of FLOWERING LOCUS M2015In: PLOS Genetics, ISSN 1553-7390, E-ISSN 1553-7404, Vol. 11, no 10, article id e1005588Article in journal (Refereed)
    Abstract [en]

    Plants integrate seasonal cues such as temperature and day length to optimally adjust their flowering time to the environment. Compared to the control of flowering before and after winter by the vernalization and day length pathways, mechanisms that delay or promote flowering during a transient cool or warm period, especially during spring, are less well understood. Due to global warming, understanding this ambient temperature pathway has gained increasing importance. In Arabidopsis thalianaFLOWERING LOCUS M (FLM) is a critical flowering regulator of the ambient temperature pathway. FLM is alternatively spliced in a temperature-dependent manner and the two predominant splice variants, FLM-ß and FLM-δ, can repress and activate flowering in the genetic background of the Athaliana reference accession Columbia-0. The relevance of this regulatory mechanism for the environmental adaptation across the entire range of the species is, however, unknown. Here, we identify insertion polymorphisms in the first intron of FLM as causative for accelerated flowering in many natural A. thaliana accessions, especially in cool (15°C) temperatures. We present evidence for a potential adaptive role of this structural variation and link it specifically to changes in the abundance of FLM-ß. Our results may allow predicting flowering in response to ambient temperatures in the Brassicaceae.

  • 34.
    Mateos, Julieta L.
    et al.
    Fundación Instituto Leloir, Instituto de Investigaciones Bioquímicas de Buenos Aires, Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Buenos Aires, Argentina; Instituto de Fisiología, Biología Molecular y Neurociencias (IFIBYNE-UBA-CONICET), Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Ciudad Universitaria, Buenos Aires, Argentina; RNA Biology and Molecular Physiology, Faculty of Biology, Bielefeld University, Bielefeld, Germany.
    Sanchez, Sabrina E.
    Fundación Instituto Leloir, Instituto de Investigaciones Bioquímicas de Buenos Aires, Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Buenos Aires, Argentina.
    Legris, Martina
    Fundación Instituto Leloir, Instituto de Investigaciones Bioquímicas de Buenos Aires, Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Buenos Aires, Argentina; Department of Molecular Biology, Max Planck Institute for Biology Tübingen, Tübingen, Germany.
    Esteve-Bruna, David
    Instituto de Biología Molecular y Celular de Plantas, CSIC-Universidad Politecnica de Valencia, Valencia, Spain.
    Torchio, Jeanette C.
    Fundación Instituto Leloir, Instituto de Investigaciones Bioquímicas de Buenos Aires, Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Buenos Aires, Argentina.
    Petrillo, Ezequiel
    Instituto de Fisiología, Biología Molecular y Neurociencias (IFIBYNE-UBA-CONICET), Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Ciudad Universitaria, Buenos Aires, Argentina.
    Goretti, Daniela
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Blanco-Touriñán, Noel
    Instituto de Biología Molecular y Celular de Plantas, CSIC-Universidad Politecnica de Valencia, Valencia, Spain.
    Seymour, Danelle K.
    Department of Molecular Biology, Max Planck Institute for Biology Tübingen, Tübingen, Germany.
    Schmid, Markus
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Weigel, Detlef
    Department of Molecular Biology, Max Planck Institute for Biology Tübingen, Tübingen, Germany.
    Alabadí, David
    Instituto de Biología Molecular y Celular de Plantas, CSIC-Universidad Politecnica de Valencia, Valencia, Spain.
    Yanovsky, Marcelo J.
    Fundación Instituto Leloir, Instituto de Investigaciones Bioquímicas de Buenos Aires, Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Buenos Aires, Argentina.
    PICLN modulates alternative splicing and light/temperature responses in plants2023In: Plant Physiology, ISSN 0032-0889, E-ISSN 1532-2548, Vol. 191, no 2, p. 1036-1051Article in journal (Refereed)
    Abstract [en]

    Plants undergo transcriptome reprograming to adapt to daily and seasonal fluctuations in light and temperature conditions. While most efforts have focused on the role of master transcription factors, the importance of splicing factors modulating these processes is now emerging. Efficient pre-mRNA splicing depends on proper spliceosome assembly, which in plants and animals requires the methylosome complex. Ion Chloride nucleotide-sensitive protein (PICLN) is part of the methylosome complex in both humans and Arabidopsis (Arabidopsis thaliana), and we show here that the human PICLN ortholog rescues phenotypes of Arabidopsis picln mutants. Altered photomorphogenic and photoperiodic responses in Arabidopsis picln mutants are associated with changes in pre-mRNA splicing that partially overlap with those in PROTEIN ARGININE METHYL TRANSFERASE5 (prmt5) mutants. Mammalian PICLN also acts in concert with the Survival Motor Neuron (SMN) complex component GEMIN2 to modulate the late steps of UsnRNP assembly, and many alternative splicing events regulated by PICLN but not PRMT5, the main protein of the methylosome, are controlled by Arabidopsis GEMIN2. As with GEMIN2 and SM PROTEIN E1/PORCUPINE (SME1/PCP), low temperature, which increases PICLN expression, aggravates morphological and molecular defects of picln mutants. Taken together, these results establish a key role for PICLN in the regulation of pre-mRNA splicing and in mediating plant adaptation to daily and seasonal fluctuations in environmental conditions.

  • 35. Mathieu, Johannes
    et al.
    Warthmann, Norman
    Kuettner, Frank
    Schmid, Markus
    Max Planck Institute for Developmental Biology, Department of Molecular Biology, Spemannstrasse 37 - 39, D - 72076 Tübingen, Germany.
    Export of FT protein from phloem companion cells is sufficient for floral induction in Arabidopsis2007In: Current Biology, ISSN 0960-9822, E-ISSN 1879-0445, Vol. 17, no 12, p. 1055-1060Article in journal (Refereed)
  • 36. Mathieu, Johannes
    et al.
    Yant, Levi J.
    Muerdter, Felix
    Kuettner, Frank
    Schmid, Markus
    Max Planck Institute for Developmental Biology, Department of Molecular Biology, Tübingen, Germany.
    Repression of Flowering by the miR172 Target SMZ2009In: PLoS biology, ISSN 1544-9173, E-ISSN 1545-7885, Vol. 7, no 7Article in journal (Refereed)
  • 37. Mirjam, Esther
    et al.
    Dohmann, Natascha
    Levesque, Mitchell Paul
    Isono, Erika
    Schmid, Markus
    Department of Developmental Genetics, Center for Plant Molecular Biology, Tübingen University, 72076 Tuebingen, Germany.
    Schwechheimer, Claus
    Auxin responses in mutants of the Arabidopsis CONSTITUTIVE PHOTOMORPHOGENIC9 signalosome2008In: Plant Physiology, ISSN 0032-0889, E-ISSN 1532-2548, Vol. 147, no 3, p. 1369-1379Article in journal (Refereed)
  • 38. Moyroud, Edwige
    et al.
    Minguet, Eugenio Gomez
    Ott, Felix
    Yant, Levi
    Pose, David
    Monniaux, Marie
    Blanchet, Sandrine
    Bastien, Olivier
    Thevenon, Emmanuel
    Weigel, Detlef
    Schmid, Markus
    Max Planck Institute for Developmental Biology, Department of Molecular Biology, 72076 Tuebingen, Germany .
    Parcy, Francois
    Prediction of Regulatory Interactions from Genome Sequences Using a Biophysical Model for the Arabidopsis LEAFY Transcription Factor2011In: The Plant Cell, ISSN 1040-4651, E-ISSN 1532-298X, Vol. 23, no 4, p. 1293-1306Article in journal (Refereed)
  • 39.
    Muralidhara, Prathibha
    et al.
    Department of Pharmaceutical Biology, Julius-von-Sachs-Institute, Biocenter. Julius-Maximilians Universität Würzburg, Würzburg, Germany.
    Weiste, Christoph
    Department of Pharmaceutical Biology, Julius-von-Sachs-Institute, Biocenter. Julius-Maximilians Universität Würzburg, Würzburg, Germany.
    Collani, Silvio
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Krischke, Markus
    Department of Pharmaceutical Biology, Julius-von-Sachs-Institute, Biocenter. Julius-Maximilians Universität Würzburg, Würzburg, Germany.
    Kreisz, Philipp
    Department of Pharmaceutical Biology, Julius-von-Sachs-Institute, Biocenter. Julius-Maximilians Universität Würzburg, Würzburg, Germany.
    Draken, Jan
    Department of Pharmaceutical Biology, Julius-von-Sachs-Institute, Biocenter. Julius-Maximilians Universität Würzburg, Würzburg, Germany.
    Feil, Regina
    Department of Metabolic networks, Max Planck Institute of Molecular Plant Physiology, Potsdam-Golm, Germany.
    Mair, Andrea
    Department of Biology, Stanford University, CA, Stanford, United States.
    Teige, Markus
    Department of Biochemistry and Cell Biology, University of Vienna, Vienna, Austria; Department of Molecular Systems Biology, University of Vienna, Vienna, Austria.
    Müller, Martin J.
    Department of Pharmaceutical Biology, Julius-von-Sachs-Institute, Biocenter. Julius-Maximilians Universität Würzburg, Würzburg, Germany.
    Schmid, Markus
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Becker, Dirk
    Institute for Molecular Plant Physiology and Biophysics, University of Würzburg, Würzburg, Germany.
    Lunn, John E.
    Department of Metabolic networks, Max Planck Institute of Molecular Plant Physiology, Potsdam-Golm, Germany.
    Rolland, Filip
    Laboratory of Molecular Plant Biology, Department of Biology, Katholieke Universiteit Leuven, Leuven, Belgium; KU Leuven Plant Institute (LPI), Heverlee-Leuven, Belgium.
    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
    Department of Pharmaceutical Biology, Julius-von-Sachs-Institute, Biocenter. Julius-Maximilians Universität Würzburg, Würzburg, Germany.
    Perturbations in plant energy homeostasis prime lateral root initiation via SnRK1-bZIP63-ARF19 signaling2021In: Proceedings of the National Academy of Sciences of the United States of America, ISSN 0027-8424, E-ISSN 1091-6490, Vol. 118, no 37, article id e2106961118Article in journal (Refereed)
    Abstract [en]

    Plants adjust their energy metabolism to continuous environmental fluctuations, resulting in a tremendous plasticity in their architecture. The regulatory circuits involved, however, remain largely unresolved. In Arabidopsis, moderate perturbations in photosynthetic activity, administered by short-term low light exposure or unexpected darkness, lead to increased lateral root (LR) initiation. Consistent with expression of low-energy markers, these treatments alter energy homeostasis and reduce sugar availability in roots. Here, we demonstrate that the LR response requires the metabolic stress sensor kinase Snf1-RELATED-KINASE1 (SnRK1), which phosphorylates the transcription factor BASIC LEUCINE ZIPPER63 (bZIP63) that directly binds and activates the promoter of AUXIN RESPONSE FACTOR19 (ARF19), a key regulator of LR initiation. Consistently, starvation-induced ARF19 transcription is impaired in bzip63 mutants. This study highlights a positive developmental function of SnRK1. During energy limitation, LRs are initiated and primed for outgrowth upon recovery. Hence, this study provides mechanistic insights into how energy shapes the agronomically important root system.

  • 40.
    Pandey, Saurabh Prakash
    et al.
    Beijing Advanced Innovation Centre for Tree Breeding by Molecular Design, College of Biological Sciences and Biotechnology, Beijing Forestry University, Beijing, China.
    Benstein, Ruben M.
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Wang, Yanwei
    Beijing Advanced Innovation Centre for Tree Breeding by Molecular Design, College of Biological Sciences and Biotechnology, Beijing Forestry University, Beijing, China.
    Schmid, Markus
    Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC). Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Beijing Advanced Innovation Centre for Tree Breeding by Molecular Design, College of Biological Sciences and Biotechnology, Beijing Forestry University, Beijing, China.
    Epigenetic regulation of temperature responses: past successes and future challenges2021In: Journal of Experimental Botany, ISSN 0022-0957, E-ISSN 1460-2431, Vol. 72, no 21, p. 7482-7497Article, review/survey (Refereed)
    Abstract [en]

    In contrast to animals, plants cannot avoid unfavorable temperature conditions. Instead, plants have evolved intricate signaling pathways that enable them to perceive and respond to temperature. General acclimation processes that prepare the plant to respond to stressful heat and cold usually occur throughout the whole plant. More specific temperature responses, however, are limited to certain tissues or cell types. While global responses are amenable to epigenomic analyses, responses that are highly localized are more problematic as the chromatin in question is not easily accessible. Here we review current knowledge of the epigenetic regulation of FLOWERING LOCUS C and FLOWERING LOCUS T as examples of temperature-responsive flowering time regulator genes that are expressed broadly throughout the plants and in specific cell types, respectively. While this work has undoubtedly been extremely successful, we reason that future analyses would benefit from higher spatiotemporal resolution. We conclude by reviewing methods and successful applications of tissue-and cell type-specific epigenomic analyses and provide a brief outlook on future single-cell epigenomics.

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  • 41. Pfeiffer, Anne
    et al.
    Janocha, Denis
    Dong, Yihan
    Medzihradszky, Anna
    Schöne, Stefanie
    Daum, Gabor
    Suzaki, Takuya
    Forner, Joachim
    Longenecker, Tobias
    Rempel, Eugen
    Schmid, Markus
    Department of Molecular Biology, Max Planck Institute for Developmental Biology, Tübingen, Germany.
    Wirtz, Markus
    Hell, Rüdiger
    Lohmann, Jan U.
    Integration of light and metabolic signals for stem cell activation at the shoot apical meristem2016In: eLIFE, E-ISSN 2050-084X, Vol. 5, article id e17023Article in journal (Refereed)
    Abstract [en]

    A major feature of embryogenesis is the specification of stem cell systems, but in contrast to the situation in most animals, plant stem cells remain quiescent until the postembryonic phase of development. Here, we dissect how light and metabolic signals are integrated to overcome stem cell dormancy at the shoot apical meristem. We show on the one hand that light is able to activate expression of the stem cell inducer WUSCHEL independently of photosynthesis and that this likely involves inter-regional cytokinin signaling. Metabolic signals, on the other hand, are transduced to the meristem through activation of the TARGET OF RAPAMYCIN (TOR) kinase. Surprisingly, TOR is also required for light signal dependent stem cell activation. Thus, the TOR kinase acts as a central integrator of light and metabolic signals and a key regulator of stem cell activation at the shoot apex.

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  • 42. Ponnu, Jathish
    et al.
    Schlereth, Armin
    Zacharaki, Vasiliki
    Działo, Magdalena A.
    Abel, Christin
    Feil, Regina
    Schmid, Markus
    Department of Molecular Biology, Max Planck Institute for Developmental Biology, Tübingen, Germany.
    Wahl, Vanessa
    The trehalose 6-phosphate pathway impacts vegetative phase change in Arabidopsis thaliana2020In: The Plant Journal, ISSN 0960-7412, E-ISSN 1365-313X, Vol. 104, no 3, p. 768-780Article in journal (Refereed)
    Abstract [en]

    The vegetative phase change marks the beginning of the adult phase in the life cycle of plants and is associated with a gradual decline in the microRNA miR156, in response to sucrose status. Trehalose 6‐phosphate (T6P) is a sugar molecule with signaling function reporting the current sucrose state. To elucidate the role of T6P signaling in vegetative phase change, molecular, genetic, and metabolic analyses were performed using Arabidopsis thaliana loss‐of‐function lines in TREHALOSE PHOSPHATE SYNTHASE1 (TPS1), a gene coding for an enzyme that catalyzes the production of T6P. These lines show a significant delay in vegetative phase change, under both short and long day conditions. Induced expression of TPS1 complements this delay in the TPS1 knockout mutant (tps1‐2 GVG::TPS1). Further analyses indicate that the T6P pathway promotes vegetative phase transition by suppressing miR156 expression and thereby modulating the levels of its target transcripts, the SQUAMOSA PROMOTER BINDING PROTEIN‐LIKE genes. TPS1 knockdown plants, with a delayed vegetative phase change phenotype, accumulate significantly more sucrose than wild‐type plants as a result of a feedback mechanism. In summary, we conclude that the T6P pathway forms an integral part of an endogenous mechanism that influences phase transitions dependent on the metabolic state.

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  • 43. Ponnu, Jathish
    et al.
    Wahl, Vanessa
    Schmid, Markus
    Max Planck Institute for Developmental Biology, Department of Molecular Biology, Tuebingen, Germany.
    Trehalose-6-phosphate: connecting plant metabolism and development2011In: Frontiers in Plant Science, E-ISSN 1664-462X, Vol. 2Article in journal (Refereed)
  • 44. Pose, David
    et al.
    Verhage, Leonie
    Ott, Felix
    Yant, Levi
    Mathieu, Johannes
    Angenent, Gerco C.
    Immink, Richard G. H.
    Schmid, Markus
    Max Planck Institute for Developmental Biology, Department of Molecular Biology, Spemannstrasse 35, 72076 Tübingen, Germany.
    Temperature-dependent regulation of flowering by antagonistic FLM variants2013In: Nature, ISSN 0028-0836, E-ISSN 1476-4687, Vol. 503, no 7476, p. 414-+Article in journal (Refereed)
  • 45. Pose, David
    et al.
    Yant, Levi
    Schmid, Markus
    Max Planck Institute for Developmental Biology, Department of Molecular Biology, Tuebingen, Germany.
    The end of innocence: flowering networks explode in complexity2012In: Current opinion in plant biology, ISSN 1369-5266, E-ISSN 1879-0356, Vol. 15, no 1, p. 45-50Article in journal (Refereed)
  • 46. Prát, Tomáš
    et al.
    Hajný, Jakub
    Grunewald, Wim
    Vasileva, Mina
    Molnár, Gergely
    Tejos, Ricardo
    Schmid, Markus
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Sauer, Michael
    Friml, Jiří
    WRKY23 is a component of the transcriptional network mediating auxin feedback on PIN polarity2018In: PLOS Genetics, ISSN 1553-7390, E-ISSN 1553-7404, Vol. 14, no 1, article id e1007177Article in journal (Refereed)
    Abstract [en]

    Auxin is unique among plant hormones due to its directional transport that is mediated by the polarly distributed PIN auxin transporters at the plasma membrane. The canalization hypothesis proposes that the auxin feedback on its polar flow is a crucial, plant-specific mechanism mediating multiple self-organizing developmental processes. Here, we used the auxin effect on the PIN polar localization in Arabidopsis thaliana roots as a proxy for the auxin feedback on the PIN polarity during canalization. We performed microarray experiments to find regulators of this process that act downstream of auxin. We identified genes that were transcriptionally regulated by auxin in an AXR3/IAA17-and ARF7/ARF19-dependent manner. Besides the known components of the PIN polarity, such as PID and PIP5K kinases, a number of potential new regulators were detected, among which the WRKY23 transcription factor, which was characterized in more detail. Gain-and loss-of-function mutants confirmed a role for WRKY23 in mediating the auxin effect on the PIN polarity. Accordingly, processes requiring auxin-mediated PIN polarity rearrangements, such as vascular tissue development during leaf venation, showed a higher WRKY23 expression and required the WRKY23 activity. Our results provide initial insights into the auxin transcriptional network acting upstream of PIN polarization and, potentially, canalization-mediated plant development.

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  • 47. Sayou, Camille
    et al.
    Nanao, Max H.
    Jamin, Marc
    Pose, David
    Thevenon, Emmanuel
    Gregoire, Laura
    Tichtinsky, Gabrielle
    Denay, Gregoire
    Ott, Felix
    Llobet, Marta Peirats
    Schmid, Markus
    Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC). Umeå University, Faculty of Science and Technology, Department of Plant Physiology.
    Dumas, Renaud
    Parcy, Francois
    A SAM oligomerization domain shapes the genomic binding landscape of the LEAFY transcription factor2016In: Nature Communications, E-ISSN 2041-1723, Vol. 7, article id 11222Article in journal (Refereed)
    Abstract [en]

    Deciphering the mechanisms directing transcription factors (TFs) to specific genome regions is essential to understand and predict transcriptional regulation. TFs recognize short DNA motifs primarily through their DNA-binding domain. Some TFs also possess an oligomerization domain suspected to potentiate DNA binding but for which the genome-wide influence remains poorly understood. Here we focus on the LEAFY transcription factor, a master regulator of flower development in angiosperms. We have determined the crystal structure of its conserved amino-terminal domain, revealing an unanticipated Sterile Alpha Motif oligomerization domain. We show that this domain is essential to LEAFY floral function. Moreover, combined biochemical and genome-wide assays suggest that oligomerization is required for LEAFY to access regions with low-affinity binding sites or closed chromatin. This finding shows that domains that do not directly contact DNA can nevertheless have a profound impact on the DNA binding landscape of a TF.

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  • 48. Schlereth, Alexandra
    et al.
    Moller, Barbara
    Liu, Weilin
    Kientz, Marika
    Flipse, Jacky
    Rademacher, Eike H.
    Schmid, Markus
    Max Planck Institute for Developmental Biology, Department of Molecular Biology, Tübingen, Germany.
    Juergens, Gerd
    Weijers, Dolf
    MONOPTEROS controls embryonic root initiation by regulating a mobile transcription factor2010In: Nature, ISSN 0028-0836, E-ISSN 1476-4687, Vol. 464, no 7290, p. 913-916Article in journal (Refereed)
    Abstract [en]

    Acquisition of cell identity in plants relies strongly on positional information1, hence cell–cell communication and inductive signalling are instrumental for developmental patterning. During Arabidopsis embryogenesis, an extra-embryonic cell is specified to become the founder cell of the primary root meristem, hypophysis, in response to signals from adjacent embryonic cells2. The auxin-dependent transcription factor MONOPTEROS (MP) drives hypophysis specification by promoting transport of the hormone auxin from the embryo to the hypophysis precursor. However, auxin accumulation is not sufficient for hypophysis specification, indicating that additional MP-dependent signals are required3. Here we describe the microarray-based isolation of MP target genes that mediate signalling from embryo to hypophysis. Of three direct transcriptional target genes, TARGET OF MP 5 (TMO5) and TMO7 encode basic helix–loop–helix (bHLH) transcription factors that are expressed in the hypophysis-adjacent embryo cells, and are required and partially sufficient for MP-dependent root initiation. Importantly, the small TMO7 transcription factor moves from its site of synthesis in the embryo to the hypophysis precursor, thus representing a novel MP-dependent intercellular signal in embryonic root specification.

  • 49.
    Schmid, M.
    et al.
    Max Planck Institute for Developmental Biology, Spemannstrasse 37-39, 72076 Tübingen, Germany.
    Davison, T. S.
    Henz, S. R.
    Pape, U. J.
    Demar, M.
    Vingron, M.
    Scholkopf, B.
    Weigel, D.
    Lohmann, J. U.
    A gene expression map of Arabidopsis thaliana development2005In: Nature Genetics, ISSN 1061-4036, E-ISSN 1546-1718, Vol. 37, no 5, p. 501-506Article in journal (Refereed)
  • 50.
    Schmid, M.
    et al.
    Lehrstuhl für Botanik, Biologikum-Weihenstephan, Technische Universität München, Am Hochanger 4, D-85350 Freising, Germany.
    Simpson, D.
    Gietl, C.
    Programmed cell death in castor bean endosperm is associated with the accumulation and release of a cysteine endopeptidase from ricinosomes1999In: Proceedings of the National Academy of Sciences of the United States of America, ISSN 0027-8424, E-ISSN 1091-6490, Vol. 96, no 24, p. 14159-14164Article in journal (Refereed)
12 1 - 50 of 73
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