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Schmid, Markus
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Publications (10 of 56) Show all publications
Speth, C., Szabo, E. X., Martinho, C., Collani, S., zur Oven-Krockhaus, S., Richter, S., . . . Laubinger, S. (2018). Arabidopsis RNA processing factor SERRATE regulates the transcription of intronless genes. eLIFE, 7, Article ID e37078.
Open this publication in new window or tab >>Arabidopsis RNA processing factor SERRATE regulates the transcription of intronless genes
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2018 (English)In: eLIFE, E-ISSN 2050-084X, Vol. 7, article id e37078Article in journal (Refereed) Published
Abstract [en]

Intron splicing increases proteome complexity, promotes RNA stability, and enhances transcription. However, introns and the concomitant need for splicing extend the time required for gene expression and can cause an undesirable delay in the activation of genes. Here, we show that the plant microRNA processing factor SERRATE (SE) plays an unexpected and pivotal role in the regulation of intronless genes. Arabidopsis SE associated with more than 1000, mainly intronless, genes in a transcription-dependent manner. Chromatin-bound SE liaised with paused and elongating polymerase II complexes and promoted their association with intronless target genes. Our results indicate that stress-responsive genes contain no or few introns, which negatively affects their expression strength, but that some genes circumvent this limitation via a novel SE-dependent transcriptional activation mechanism. Transcriptome analysis of a Drosophila mutant defective in ARS2, the metazoan homologue of SE, suggests that SE/ARS2 function in regulating intronless genes might be conserved across kingdoms.

Place, publisher, year, edition, pages
Elife Sciences Publications ltd, 2018
National Category
Biochemistry and Molecular Biology
Identifiers
urn:nbn:se:umu:diva-152270 (URN)10.7554/eLife.37078 (DOI)000444379000001 ()30152752 (PubMedID)
Available from: 2018-10-03 Created: 2018-10-03 Last updated: 2018-10-03Bibliographically approved
Capovilla, G., Delhomme, N., Collani, S., Shutava, I., Bezrukov, I., Symeonidi, E., . . . Schmid, M. (2018). PORCUPINE regulates development in response to temperature through alternative splicing. Nature plants, 4(8), 534-539
Open this publication in new window or tab >>PORCUPINE regulates development in response to temperature through alternative splicing
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2018 (English)In: Nature plants, ISSN 2055-026X, Vol. 4, no 8, p. 534-539Article in journal (Refereed) Published
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.

Place, publisher, year, edition, pages
Nature Publishing Group, 2018
National Category
Biochemistry and Molecular Biology Botany
Identifiers
urn:nbn:se:umu:diva-152230 (URN)10.1038/s41477-018-0176-z (DOI)000443861300009 ()29988152 (PubMedID)
Available from: 2018-10-25 Created: 2018-10-25 Last updated: 2018-10-25Bibliographically approved
Shanks, C. M., Hecker, A., Cheng, C.-Y., Brand, L., Collani, S., Schmid, M., . . . Kieber, J. J. (2018). Role of BASIC PENTACYSTEINE transcription factors in a subset of cytokinin signaling responses. The Plant Journal, 95(3), 458-473
Open this publication in new window or tab >>Role of BASIC PENTACYSTEINE transcription factors in a subset of cytokinin signaling responses
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2018 (English)In: The Plant Journal, ISSN 0960-7412, E-ISSN 1365-313X, Vol. 95, no 3, p. 458-473Article in journal (Refereed) Published
Abstract [en]

Cytokinin plays diverse roles in plant growth and development, generally acting by modulating gene transcription in target tissues. The type-B Arabidopsis response regulators (ARR) transcription factors have emerged as primary targets of cytokinin signaling and are required for essentially all cytokinin-mediated changes in gene expression. The diversity of cytokinin function is likely imparted by the activity of various transcription factors working with the type-B ARRs to alter specific sets of target genes. One potential set of co-regulators modulating the cytokinin response are the BARLEY B-RECOMBINANT/BASIC PENTACYSTEINE (BBR/BPC) family of plant-specific transcription factors. Here, we show that disruption of multiple BPCs results in reduced sensitivity to cytokinin. Further, the BPCs are necessary for the induction of a subset of genes in response to cytokinin. We identified direct invivo targets of BPC6 using ChIP-Seq and found an enrichment of promoters of genes differentially expressed in response to cytokinin. Further, a significant number of BPC6 regulated genes are also direct targets of the type-B ARRs. Potential cis-binding elements for a number of other transcription factors linked to cytokinin action are enriched in the BPC binding fragments, including those for the cytokinin response factors (CRFs). In addition, several BPCs interact with a subset of type-A ARRs. Consistent with these results, a significant number of genes whose expression is altered in bpc mutant roots are also mis-expressed in crf1,3,5,6 and type-A arr3,4,5,6,7,8,9,15 mutant roots. These results suggest that the BPCs are part of a complex network of transcription factors that are involved in the response to cytokinin.

Place, publisher, year, edition, pages
John Wiley & Sons, 2018
Keywords
Arabidopsis thaliana, ChIP-Seq, cytokinin, phytohormones, transcription factor
National Category
Biochemistry and Molecular Biology
Identifiers
urn:nbn:se:umu:diva-150658 (URN)10.1111/tpj.13962 (DOI)000438224100006 ()29763523 (PubMedID)
Available from: 2018-08-28 Created: 2018-08-28 Last updated: 2018-08-28Bibliographically approved
Prát, T., Hajný, J., Grunewald, W., Vasileva, M., Molnár, G., Tejos, R., . . . Friml, J. (2018). WRKY23 is a component of the transcriptional network mediating auxin feedback on PIN polarity. PLoS Genetics, 14(1), Article ID e1007177.
Open this publication in new window or tab >>WRKY23 is a component of the transcriptional network mediating auxin feedback on PIN polarity
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2018 (English)In: PLoS Genetics, ISSN 1553-7390, E-ISSN 1553-7404, Vol. 14, no 1, article id e1007177Article in journal (Refereed) Published
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.

Place, publisher, year, edition, pages
PUBLIC LIBRARY SCIENCE, 2018
National Category
Developmental Biology
Identifiers
urn:nbn:se:umu:diva-144963 (URN)10.1371/journal.pgen.1007177 (DOI)000423718600034 ()
Available from: 2018-02-21 Created: 2018-02-21 Last updated: 2018-06-09Bibliographically approved
Conn, V. M., Hugouvieux, V., Nayak, A., Conos, S. A., Capovilla, G., Cildir, G., . . . Conn, S. J. (2017). A circRNA from SEPALLATA3 regulates splicing of its cognate mRNA through R-loop formation. Nature Plants, 3(5), Article ID 17053.
Open this publication in new window or tab >>A circRNA from SEPALLATA3 regulates splicing of its cognate mRNA through R-loop formation
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2017 (English)In: Nature Plants, ISSN 2055-026X, Vol. 3, no 5, article id 17053Article in journal (Refereed) Published
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.

Place, publisher, year, edition, pages
Nature Publishing Group, 2017
National Category
Biochemistry and Molecular Biology
Identifiers
urn:nbn:se:umu:diva-137882 (URN)10.1038/nplants.2017.53 (DOI)000404896700006 ()28418376 (PubMedID)
Available from: 2017-08-10 Created: 2017-08-10 Last updated: 2018-06-09Bibliographically approved
Capovilla, G., Symeonidi, E., Wu, R. & Schmid, M. (2017). Contribution of major FLM isoforms to temperature-dependent flowering in Arabidopsis thaliana. Journal of Experimental Botany, 68(18), 5117-5127
Open this publication in new window or tab >>Contribution of major FLM isoforms to temperature-dependent flowering in Arabidopsis thaliana
2017 (English)In: Journal of Experimental Botany, ISSN 0022-0957, E-ISSN 1460-2431, Vol. 68, no 18, p. 5117-5127Article in journal (Refereed) Published
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.

Place, publisher, year, edition, pages
Oxford University Press, 2017
Keywords
Arabidopsis thaliana, CRISPR/Cas9, FLOWERING LOCUS M (FLM), flowering time, splice isoforms, temperature-dependent alternative splicing
National Category
Genetics and Breeding in Agricultural Sciences
Identifiers
urn:nbn:se:umu:diva-142004 (URN)10.1093/jxb/erx328 (DOI)000414371700011 ()29036339 (PubMedID)
Available from: 2017-11-21 Created: 2017-11-21 Last updated: 2018-06-09Bibliographically approved
Ahn, J. H. & Schmid, M. (2017). Editorial overview: Growth and development: Change is in the air: how plants modulate development in response to the environment. Current opinion in plant biology, 35, IV-VI
Open this publication in new window or tab >>Editorial overview: Growth and development: Change is in the air: how plants modulate development in response to the environment
2017 (English)In: Current opinion in plant biology, ISSN 1369-5266, E-ISSN 1879-0356, Vol. 35, p. IV-VIArticle in journal, Editorial material (Refereed) Published
Place, publisher, year, edition, pages
CURRENT BIOLOGY LTD, 2017
National Category
Biological Sciences
Identifiers
urn:nbn:se:umu:diva-133433 (URN)10.1016/j.pbi.2017.01.003 (DOI)000396959300001 ()28162929 (PubMedID)
Available from: 2017-04-21 Created: 2017-04-21 Last updated: 2018-06-09Bibliographically approved
You, Y., Sawikowska, A., Neumann, M., Pose, D., Capovilla, G., Langenecker, T., . . . Schmid, M. (2017). Temporal dynamics of gene expression and histone marks at the Arabidopsis shoot meristem during flowering. Nature Communications, 8, Article ID 15120.
Open this publication in new window or tab >>Temporal dynamics of gene expression and histone marks at the Arabidopsis shoot meristem during flowering
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2017 (English)In: Nature Communications, ISSN 2041-1723, E-ISSN 2041-1723, Vol. 8, article id 15120Article in journal (Refereed) Published
Abstract [en]

Plants can produce organs throughout their entire life from pluripotent stem cells located at their growing tip, the shoot apical meristem (SAM). At the time of flowering, the SAM of Arabidopsis thaliana switches fate and starts producing flowers instead of leaves. Correct timing of flowering in part determines reproductive success, and is therefore under environmental and endogenous control. How epigenetic regulation contributes to the floral transition has eluded analysis so far, mostly because of the poor accessibility of the SAM. Here we report the temporal dynamics of the chromatin modifications H3K4me3 and H3K27me3 and their correlation with transcriptional changes at the SAM in response to photoperiod-induced flowering. Emphasizing the importance of tissue-specific epigenomic analyses we detect enrichments of chromatin states in the SAM that were not apparent in whole seedlings. Furthermore, our results suggest that regulation of translation might be involved in adjusting meristem function during the induction of flowering.

Place, publisher, year, edition, pages
Nature Publishing Group, 2017
National Category
Botany Developmental Biology
Identifiers
urn:nbn:se:umu:diva-136055 (URN)10.1038/ncomms15120 (DOI)000401508700001 ()28513600 (PubMedID)
Available from: 2017-06-20 Created: 2017-06-20 Last updated: 2018-06-09Bibliographically approved
Sayou, C., Nanao, M. H., Jamin, M., Pose, D., Thevenon, E., Gregoire, L., . . . Parcy, F. (2016). A SAM oligomerization domain shapes the genomic binding landscape of the LEAFY transcription factor. Nature Communications, 7, Article ID 11222.
Open this publication in new window or tab >>A SAM oligomerization domain shapes the genomic binding landscape of the LEAFY transcription factor
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2016 (English)In: Nature Communications, ISSN 2041-1723, E-ISSN 2041-1723, Vol. 7, article id 11222Article in journal (Refereed) Published
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.

National Category
Cell Biology
Identifiers
urn:nbn:se:umu:diva-121484 (URN)10.1038/ncomms11222 (DOI)000374573500001 ()27097556 (PubMedID)
Available from: 2016-06-17 Created: 2016-06-02 Last updated: 2018-06-07Bibliographically approved
Pfeiffer, A., Janocha, D., Dong, Y., Medzihradszky, A., Schöne, S., Daum, G., . . . Lohmann, J. U. (2016). Integration of light and metabolic signals for stem cell activation at the shoot apical meristem. eLIFE, 5, Article ID e17023.
Open this publication in new window or tab >>Integration of light and metabolic signals for stem cell activation at the shoot apical meristem
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2016 (English)In: eLIFE, E-ISSN 2050-084X, Vol. 5, article id e17023Article in journal (Refereed) Published
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.

Place, publisher, year, edition, pages
eLife Sciences, 2016
National Category
Biological Sciences
Identifiers
urn:nbn:se:umu:diva-125555 (URN)10.7554/eLife.17023 (DOI)000380853400001 ()
Available from: 2016-09-14 Created: 2016-09-13 Last updated: 2018-06-07Bibliographically approved
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