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  • 1.
    Alvarez, Jose M.
    et al.
    Swedish Univ Agr Sci, Uppsala BioCtr, Dept Plant Biol, SE-75007 Uppsala, Sweden.;Linnean Ctr Plant Biol, SE-75007 Uppsala, Sweden..
    Sohlberg, Joel
    Swedish Univ Agr Sci, Uppsala BioCtr, Dept Plant Biol, SE-75007 Uppsala, Sweden.;Linnean Ctr Plant Biol, SE-75007 Uppsala, Sweden..
    Engström, Peter
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany.
    Zhu, Tianqing
    Swedish Univ Agr Sci, Uppsala BioCtr, Dept Plant Biol, SE-75007 Uppsala, Sweden.;Linnean Ctr Plant Biol, SE-75007 Uppsala, Sweden..
    Englund, Marie
    Linnean Ctr Plant Biol, SE-75007 Uppsala, Sweden.;Uppsala Univ, Dept Organismal Biol, Physiol Bot, SE-75007 Uppsala, Sweden..
    Moschou, Panagiotis N.
    Swedish Univ Agr Sci, Uppsala BioCtr, Dept Plant Biol, SE-75007 Uppsala, Sweden.;Linnean Ctr Plant Biol, SE-75007 Uppsala, Sweden..
    von Arnold, Sara
    Swedish Univ Agr Sci, Uppsala BioCtr, Dept Plant Biol, SE-75007 Uppsala, Sweden.;Linnean Ctr Plant Biol, SE-75007 Uppsala, Sweden..
    The WUSCHEL-RELATED HOMEOBOX 3 gene PaWOX3 regulates lateral organ formation in Norway spruce2015In: New Phytologist, ISSN 0028-646X, E-ISSN 1469-8137, Vol. 208, no 4, p. 1078-1088Article in journal (Refereed)
    Abstract [en]

    In angiosperms, WUSCHEL-RELATED HOMEOBOX 3 (WOX3) genes are required for the recruitment of founder cells from the lateral domains of shoot meristems that form lateral regions of leaves. However, the regulation of the formation of lateral organs in gymnosperms remains unknown. By using somatic embryos of Norway spruce ( Picea abies) we have studied the expression and function of PaWOX3 during embryo development. The mRNA abundance of PaWOX3 was determined by quantitative real-time PCR, and the spatial expression of PaWOX3 was analysed by histochemical beta-glucuronidase (GUS) assays and in situ mRNA hybridization. To investigate the function of PaWOX3, we analysed how downregulation of PaWOX3 in RNA interference lines affected embryo development and morphology. PaWOX3 was highly expressed in mature embryos at the base of each cotyledon close to the junction between the cotyledons, and in the lateral margins of cotyledons and needles, separating them into an adaxial and an abaxial side. Downregulation of the expression of PaWOX3 caused defects in lateral margin outgrowth in cotyledons and needles, and reduced root elongation. Our data suggest that the WOX3 function in margin outgrowth in lateral organs is conserved among the seed plants, whereas its function in root elongation may be unique to gymnosperms.

  • 2.
    Burraco, Pablo
    et al.
    CSIC, Donana Biol Stn, Dept Wetland Ecol, Ecol Evolut & Dev Grp, E-41092 Seville, Spain..
    Valdes, Ana Elisa
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany. Stockholm Univ, Dept Ecol Environm & Plant Sci, SE-10691 Stockholm, Sweden..
    Johansson, Frank
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics.
    Gomez-Mestre, Ivan
    CSIC, Donana Biol Stn, Dept Wetland Ecol, Ecol Evolut & Dev Grp, E-41092 Seville, Spain..
    Physiological mechanisms of adaptive developmental plasticity in Rana temporaria island populations2017In: BMC Evolutionary Biology, ISSN 1471-2148, E-ISSN 1471-2148, Vol. 17, article id 164Article in journal (Refereed)
    Abstract [en]

    Background: Adaptive plasticity is essential for many species to cope with environmental heterogeneity. In particular, developmental plasticity allows organisms with complex life cycles to adaptively adjust the timing of ontogenetic switch points. Size at and time to metamorphosis are reliable fitness indicators in organisms with complex cycles. The physiological machinery of developmental plasticity commonly involves the activation of alternative neuroendocrine pathways, causing metabolic alterations. Nevertheless, we have still incomplete knowledge about how these mechanisms evolve under environments that select for differences in adaptive plasticity. In this study, we investigate the physiological mechanisms underlying divergent degrees of developmental plasticity across Rana temporaria island populations inhabiting different types of pools in northern Sweden. Methods: In a laboratory experiment we estimated developmental plasticity of amphibian larvae from six populations coming from three different island habitats: islands with only permanent pools, islands with only ephemeral pools, and islands with a mixture of both types of pools. We exposed larvae of each population to either constant water level or simulated pool drying, and estimated their physiological responses in terms of corticosterone levels, oxidative stress, and telomere length. Results: We found that populations from islands with only temporary pools had a higher degree of developmental plasticity than those from the other two types of habitats. All populations increased their corticosterone levels to a similar extent when subjected to simulated pool drying, and therefore variation in secretion of this hormone does not explain the observed differences among populations. However, tadpoles from islands with temporary pools showed lower constitutive activities of catalase and glutathione reductase, and also showed overall shorter telomeres. Conclusions: The observed differences are indicative of physiological costs of increased developmental plasticity, suggesting that the potential for plasticity is constrained by its costs. Thus, high levels of responsiveness in the developmental rate of tadpoles have evolved in islands with pools at high but variable risk of desiccation. Moreover, the physiological alterations observed may have important consequences for both short-term odds of survival and long term effects on lifespan.

  • 3.
    Carlsbecker, Annelie
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany.
    Sundstrom, Jens F.
    Englund, Marie
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany.
    Uddenberg, Daniel
    Izquierdo, Liz
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology.
    Kvarnheden, Anders
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology.
    Vergara-Silva, Francisco
    Engström, Peter
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany.
    Molecular control of normal and acrocona mutant seed cone development in Norway spruce (Picea abies) and the evolution of conifer ovule-bearing organs2013In: New Phytologist, ISSN 0028-646X, E-ISSN 1469-8137, Vol. 200, no 1, p. 261-275Article in journal (Refereed)
    Abstract [en]

    Reproductive organs in seed plants are morphologically divergent and their evolutionary history is often unclear. The mechanisms controlling their development have been extensively studied in angiosperms but are poorly understood in conifers and other gymnosperms. Here, we address the molecular control of seed cone development in Norway spruce, Picea abies. We present expression analyses of five novel MADS-box genes in comparison with previously identified MADS and LEAFY genes at distinct developmental stages. In addition, we have characterized the homeotic transformation from vegetative shoot to female cone and associated changes in regulatory gene expression patterns occurring in the acrocona mutant. The analyses identified genes active at the onset of ovuliferous and ovule development and identified expression patterns marking distinct domains of the ovuliferous scale. The reproductive transformation in acrocona involves the activation of all tested genes normally active in early cone development, except for an AGAMOUS-LIKE6/SEPALLATA (AGL6/SEP) homologue. This absence may be functionally associated with the nondeterminate development of the acrocona ovule-bearing scales. Our morphological and gene expression analyses give support to the hypothesis that the modern cone is a complex structure, and the ovuliferous scale the result of reductions and compactions of an ovule-bearing axillary short shoot in cones of Paleozoic conifers.

  • 4.
    Carlsbecker, Annelie
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Evolutionary Biology. Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany.
    Sundström, Jens
    Tandre, Karolina
    Englund, Marie
    Kvarnheden, Anders
    Johansson, Urban
    Engström, Peter
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany.
    The DAL10 gene from Norway spruce (Picea abies) belongs to a potentially gymnosperm-specific subclass of MADS-box genes and is specifically active in seed cones and pollen cones.2003In: Evolution & Development, Vol. 5, no 6, p. 551-561Article in journal (Refereed)
  • 5.
    Carlsbecker, Annelie
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Evolution, Genomics and Systematics. Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany. Fysiologisk botanik.
    Tandre, Karolina
    Johansson, Urban
    Englund, Marie
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Evolution, Genomics and Systematics. Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany. Fysiologisk botanik.
    Engström, Peter
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Evolution, Genomics and Systematics. Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany. Fysiologisk botanik.
    The MADS-box gene DAL1 is a potential mediator of the juvenile-to-adult transition in Norway spruce (Picea abies)2004In: The Plant Journal, Vol. 40, p. 546-557Article in journal (Refereed)
    Abstract [en]

    Progression through the plant life cycle involves changes in many essential features, most notably in the capacity to reproduce. The transition from juvenile vegetative and non-reproductive to an adult reproductive phase is gradual and can take many years; in the conifer Norway spruce, Picea abiea, typically 20-25 years. We present a detailed analysis of the activities of three regulatory genes with potential roles in the transition in Norway spruce: DAL1, a MADS-box gene related to the AGL6 group of genes from angiosperms, and the two LEAFY-related genes PaLFY and PaNLY. DAL1 activity is initiated in the shoots of juvenile trees at an age of 3-5 years, and then increases with age, whereas both LFY genes are active throughout the juvenile phase. The activity of DAL1 further shows a spatial pattern along the stem of the tree that parallels a similar gradient in physiolpoical and morphological features associated with maturation to the adult phase. Constitutive expression of DAL1 in transgenic Arabidopsis plants caused a dramatic attenuation of both juvenile and adult growth phases;flowers forming immediately after the embryogenic phase of development in severely affected plants. Taken together, our resulsts support the notion that DAL1 may have a regulatory role in the juvenile-to-adult transition in Norway spruce.

  • 6. de Vries, Jan
    et al.
    Fischer, Angela Melanie
    Roettger, Mayo
    Rommel, Sophie
    Schluepmann, Henriette
    Bräutigam, Andrea
    Carlsbecker, Annelie
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany.
    Gould, Sven Bernhard
    Cytokinin-induced promotion of root meristem size in the fern Azolla supports a shoot-like origin of euphyllophyte roots.2016In: New Phytologist, ISSN 0028-646X, E-ISSN 1469-8137, Vol. 209, no 2, p. 705-720Article in journal (Refereed)
    Abstract [en]

    The phytohormones cytokinin and auxin orchestrate the root meristem development in angiosperms by determining embryonic bipolarity. Ferns, having the most basal euphyllophyte root, form neither bipolar embryos nor permanent embryonic primary roots but rather an adventitious root system. This raises the questions of how auxin and cytokinin govern fern root system architecture and whether this can tell us something about the origin of that root. Using Azolla filiculoides, we characterized the influence of IAA and zeatin on adventitious fern root meristems and vasculature by Nomarski microscopy. Simultaneously, RNAseq analyses, yielding 36 091 contigs, were used to uncover how the phytohormones affect root tip gene expression. We show that auxin restricts Azolla root meristem development, while cytokinin promotes it; it is the opposite effect of what is observed in Arabidopsis. Global gene expression profiling uncovered 145 genes significantly regulated by cytokinin or auxin, including cell wall modulators, cell division regulators and lateral root formation coordinators. Our data illuminate both evolution and development of fern roots. Promotion of meristem size through cytokinin supports the idea that root meristems of euphyllophytes evolved from shoot meristems. The foundation of these roots was laid in a postembryonically branching shoot system.

  • 7.
    Englund, Marie
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany.
    Carlsbecker, Annelie
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany.
    Engström, Peter
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany.
    Vergara-Silva, Francisco
    Morphological "primary homology" and expression of AG -subfamily MADS-box genes in pines, podocarps, and yews2011In: Evolution & Development, ISSN 1520-541X, E-ISSN 1525-142X, Vol. 13, no 2, p. 171-181Article in journal (Refereed)
    Abstract [en]

    The morphological variation among reproductive organs of extant gymnosperms is remarkable, especially among conifers. Several hypotheses concerning morphological homology between various conifer reproductive organs have been put forward, in particular in relation to the pine ovuliferous scale. Here, we use the expression patterns of orthologs of the ABC-model MADS-box gene AGAMOUS (AG) for testing morphological homology hypotheses related to organs of the conifer female cone. To this end, we first developed a tailored 3'RACE procedure that allows reliable amplification of partial sequences highly similar to gymnosperm-derived members of the AG-subfamily of MADS-box genes. Expression patterns of two novel conifer AG orthologs cloned with this procedure-namely PodAG and TgAG, obtained from the podocarp Podocarpus reichei and the yew Taxus globosa, respectively-are then further characterized in the morphologically divergent female cones of these species. The expression patterns of PodAG and TgAG are compared with those of DAL2, a previously discovered Picea abies (Pinaceae) AG ortholog. By treating the expression patterns of DAL2, PodAG, and TgAG as character states mapped onto currently accepted cladogram topologies, we suggest that the epimatium-that is, the podocarp female cone organ previously postulated as a "modified" ovuliferous scale-and the canonical Pinaceae ovuliferous scale can be legitimally conceptualized as "primary homologs." Character state mapping for TgAG suggests in turn that the aril of Taxaceae should be considered as a different type of organ. This work demonstrates how the interaction between developmental-genetic data and formal cladistic theory could fruitfully contribute to gymnosperm systematics.

  • 8.
    Englund, Marie
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany.
    Carlsbecker, Annelie
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany.
    Engström, Peter
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany.
    Vergara-Silva, Francisco
    Morphological "primary homology" and expression of AG -subfamily MADS-box genes in pines, podocarps, and yews2011In: Evolution & Development, ISSN 1520-541X, E-ISSN 1525-142X, Vol. 13, no 2, p. 171-181Article in journal (Refereed)
    Abstract [en]

    The morphological variation among reproductive organs of extant gymnosperms is remarkable, especially among conifers. Several hypotheses concerning morphological homology between various conifer reproductive organs have been put forward, in particular in relation to the pine ovuliferous scale. Here, we use the expression patterns of orthologs of the ABC-model MADS-box gene AGAMOUS (AG) for testing morphological homology hypotheses related to organs of the conifer female cone. To this end, we first developed a tailored 3'RACE procedure that allows reliable amplification of partial sequences highly similar to gymnosperm-derived members of the AG-subfamily of MADS-box genes. Expression patterns of two novel conifer AG orthologs cloned with this procedure-namely PodAG and TgAG, obtained from the podocarp Podocarpus reichei and the yew Taxus globosa, respectively-are then further characterized in the morphologically divergent female cones of these species. The expression patterns of PodAG and TgAG are compared with those of DAL2, a previously discovered Picea abies (Pinaceae) AG ortholog. By treating the expression patterns of DAL2, PodAG, and TgAG as character states mapped onto currently accepted cladogram topologies, we suggest that the epimatium-that is, the podocarp female cone organ previously postulated as a "modified" ovuliferous scale-and the canonical Pinaceae ovuliferous scale can be legitimally conceptualized as "primary homologs." Character state mapping for TgAG suggests in turn that the aril of Taxaceae should be considered as a different type of organ. This work demonstrates how the interaction between developmental-genetic data and formal cladistic theory could fruitfully contribute to gymnosperm systematics.

  • 9.
    Grossmann, Jonas
    et al.
    Funct Genom Ctr Zurich, Zurich, Switzerland..
    Fernandez, Helena
    Univ Oviedo, Dept Organisms & Syst Biol BOS, Area Plant Physiol, Oviedo, Spain..
    Chaubey, Pururawa M.
    Univ Zurich, Inst Plant & Microbial Biol, Zurich Basel Plant Sci Ctr, Zurich, Switzerland.;Hadron Finsys GmbH, Pharma & Life Sci, Cham, Switzerland..
    Valdés, Ana Elisa
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany. Linnean Ctr Plant Biol, Uppsala, Sweden.; Stockholm Univ, Dept Ecol Environm & Plant Sci, Stockholm, Sweden..
    Gagliardini, Valeria
    Univ Zurich, Inst Plant & Microbial Biol, Zurich Basel Plant Sci Ctr, Zurich, Switzerland..
    Canal, Maria J.
    Univ Oviedo, Dept Organisms & Syst Biol BOS, Area Plant Physiol, Oviedo, Spain..
    Russo, Giancarlo
    Funct Genom Ctr Zurich, Zurich, Switzerland..
    Grossniklaus, Ueli
    Univ Zurich, Inst Plant & Microbial Biol, Zurich Basel Plant Sci Ctr, Zurich, Switzerland..
    Proteogenomic Analysis Greatly Expands the Identification of Proteins Related to Reproduction in the Apogamous Fern Dryopteris affinis ssp affinis2017In: Frontiers in Plant Science, ISSN 1664-462X, E-ISSN 1664-462X, Vol. 8, article id 336Article in journal (Refereed)
    Abstract [en]

    Performing proteomic studies on non-model organisms with little or no genomic information is still difficult. However, many specific processes and biochemical pathways occur only in species that are poorly characterized at the genomic level. For example, many plants can reproduce both sexually and asexually, the first one allowing the generation of new genotypes and the latter their fixation. Thus, both modes of reproduction are of great agronomic value. However, the molecular basis of asexual reproduction is not well understood in any plant. In ferns, it combines the production of unreduced spores (diplospory) and the formation of sporophytes from somatic cells (apogamy). To set the basis to study these processes, we performed transcriptomics by next-generation sequencing (NGS) and shotgun proteomics by tandem mass spectrometry in the apogamous fern D. affinis ssp. affinis. For protein identification we used the public viridiplantae database (VPDB) to identify orthologous proteins from other plant species and new transcriptomics data to generate a "species-specific transcriptome database" (SSTDB). In total 1,397 protein clusters with 5,865 unique peptide sequences were identified (13 decoy proteins out of 1,410, protFDR 0.93% on protein cluster level). We show that using the SSTDB for protein identification increases the number of identified peptides almost four times compared to using only the publically available VPDB. We identified homologs of proteins involved in reproduction of higher plants, including proteins with a potential role in apogamy. With the increasing availability of genomic data from non -model species, similar proteogenomics approaches will improve the sensitivity in protein identification for species only distantly related to models.

  • 10.
    Grossmann, Jonas
    et al.
    Functional Genomics Center, Zurich.
    Fernandez, Helena
    University of Oviedo, Spain.
    Pururawa, Mayank
    Institute of Plant Biology & Zurich-Basel Plant Science Center, University of Zurich .
    Gagliardini, Valeria
    Institute of Plant Biology & Zurich-Basel Plant Science Center, University of Zurich .
    Valdés, Ana Elisa
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany.
    Schob, Hans Peter
    Rivera, Alejandro
    Grossniklaus, Ueli
    Institute of Plant Biology & Zurich-Basel Plant Science Center, University of Zurich .
    Transcriptome vs proteome in the diploid apogamous fern Dryopteris affinis ssp. Affinis2014Conference paper (Other academic)
  • 11.
    Groth, Erika
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organism Biology, Physiological Botany.
    Functional Diversification among MADS-Box Genes and the Evolution of Conifer Seed Cone Development2010Doctoral thesis, comprehensive summary (Other academic)
    Abstract [en]

    MADS-box genes are important regulators of reproductive development in seed plants, including both flowering plants and conifers. In this thesis the evolution of the AGAMOUS subfamily of MADS-box genes, and what the ancestral function of this group of genes might have been in the early seed plants about 300 million years ago, was addressed by the discovery of two novel conifer genes, both basal to all previously known AGAMOUS subfamily genes. DAL20, the most basal of these genes, was exclusively expressed in roots, unlike all previously known AGAMOUS subfamily genes. I also studied the evolutionary mechanisms leading to functional diversification of duplicated genes in two different subfamilies of MADS-box genes; the AGAMOUS and AGL6 subfamilies. Focus was on studying changes in gene expression pattern, representing changes in the transcriptional regulation between the genes, and on comparing the functional properties of the gene products, representing changes in the protein-coding sequence between the genes. Duplicated genes in the AGL6 subfamily were found to have evolved by both mechanisms. In the AGAMOUS subfamily I found duplicated spruce genes; DAL2 and DAL20, that appear to have functionally diversified mainly by changes in the transcriptional regulation. Conifer AGAMOUS subfamily genes were also used in a comparative developmental-genetics approach to evaluate hypotheses, based on the morphology of fossil and extant conifer seed cones, on the identity of the female reproductive organ, the ovuliferous scale, and the evolution of seed cone morphology in the conifer families Pinaceae, Taxodiaceae and Cupressaceae. Seed cones in these families have been hypothesized to have homologous ovule-bearing organs, but I found substantial differences in the expression patterns of orthologous AGAMOUS subfamily genes in seed cones of these families that are not compatible with this hypothesis, indicating that the evolutionary history of conifer seed cones is more diverse than previously thought.

    List of papers
    1. AGAMOUS subfamily MADS-box genes and the evolution of seed cone morphology in Cupressaceae and Taxodiaceae
    Open this publication in new window or tab >>AGAMOUS subfamily MADS-box genes and the evolution of seed cone morphology in Cupressaceae and Taxodiaceae
    2011 (English)In: Evolution & Development, ISSN 1520-541X, E-ISSN 1525-142X, Vol. 13, no 2, p. 159-170Article in journal (Refereed) Published
    Abstract [en]

    In this comparative developmental genetics study, we test hypotheses based on fossil and morphological data on reproductive organ morphology and evolution in conifers-specifically, the ovule-bearing organ in Cupressaceae and Taxodiaceae. Genes homologous to the Arabidopsis gene AGAMOUS are expressed in ovuliferous scales of spruces (Picea) throughout development. Previous studies have shown that the AGAMOUS subfamily of MADS-box genes predates the split between angiosperms and gymnosperms, and that these genes have in part conserved functions in reproductive development among seed plants, especially in the specification of identity of the ovule-bearing organs. These data indicate that their expression in conifer families other than Pinaceae might be used as markers for organs homologous to the Pinaceae ovuliferous scale. Here we have isolated putative AGAMOUS orthologs from Cupressaceae and Taxodiaceae and analyzed their expression pattern in seed cones to test for the presence of morphological homologs of ovuliferous scales. Our results were not congruent with the hypothesis that the tooth of the Cryptomeria seed cone is homologous to the Picea ovuliferous scale. Likewise, the hypothesis that the bracts of Thujopsis and Juniperus contain fused ovuliferous scales was not supported. However, we found expression of AGAMOUS homologs in the sterile bracts of Cupressaceae seed cones at late developmental stages. This expression probably represents a novel gene function in these conifer families, since no corresponding expression has been identified in Pinaceae. Our study suggests that the evolutionary history of modern conifer cones is more diverse than previously thought.

    Keywords
    AGAMOUS, MADS-box, Cupressaceae, Taxodiaceae, conifer, evo-devo, Cryptomeria, Juniperus, Thujopsis
    National Category
    Biological Sciences
    Identifiers
    urn:nbn:se:uu:diva-128887 (URN)10.1111/j.1525-142X.2011.00466.x (DOI)000288502600005 ()21410872 (PubMedID)
    Available from: 2010-07-31 Created: 2010-07-31 Last updated: 2017-12-12Bibliographically approved
    2. Identification and characterization of basal AGAMOUS subfamily MADS-box genes from Norway spruce (Picea abies); implications for the evolution of AGAMOUS subfamily genes in seed plants
    Open this publication in new window or tab >>Identification and characterization of basal AGAMOUS subfamily MADS-box genes from Norway spruce (Picea abies); implications for the evolution of AGAMOUS subfamily genes in seed plants
    (English)Manuscript (preprint) (Other academic)
    Identifiers
    urn:nbn:se:uu:diva-128888 (URN)
    Available from: 2010-08-02 Created: 2010-07-31 Last updated: 2010-08-30
    3. Molecular and functional evolution of the AGAMOUS subfamily MADS-domain proteins
    Open this publication in new window or tab >>Molecular and functional evolution of the AGAMOUS subfamily MADS-domain proteins
    (English)Manuscript (preprint) (Other academic)
    Identifiers
    urn:nbn:se:uu:diva-128890 (URN)
    Available from: 2010-08-04 Created: 2010-07-31 Last updated: 2010-08-30
    4. Functional divergence by multiple mechanisms between the paralogous sister genes DAL1 and DAL14 in the AGL6 subfamily of MADS-box genes in the conifer Picea abies
    Open this publication in new window or tab >>Functional divergence by multiple mechanisms between the paralogous sister genes DAL1 and DAL14 in the AGL6 subfamily of MADS-box genes in the conifer Picea abies
    (English)Manuscript (preprint) (Other academic)
    Identifiers
    urn:nbn:se:uu:diva-128889 (URN)
    Available from: 2010-08-04 Created: 2010-07-31 Last updated: 2016-04-25
  • 12.
    Groth, Erika
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany.
    Carlsbecker, Annelie
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany.
    Tandre, Karolina
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany.
    Engström, Peter
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany.
    Functional divergence by multiple mechanisms between the paralogous sister genes DAL1 and DAL14 in the AGL6 subfamily of MADS-box genes in the conifer Picea abiesManuscript (preprint) (Other academic)
  • 13.
    Groth, Erika
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organism Biology, Physiological Botany.
    Engström, Peter
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organism Biology, Physiological Botany.
    Evolutionary conservation of protein-protein interaction ability in MIKC and Malpha MADS-box transcription factors in seed plantsManuscript (preprint) (Other academic)
  • 14.
    Groth, Erika
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organism Biology, Physiological Botany.
    Tandre, Karolina
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organism Biology, Physiological Botany.
    Engström, Peter
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organism Biology, Physiological Botany.
    Conservation of alternative splicing in TM3-like MIKC-type MADS-domain transcription factors in conifersManuscript (preprint) (Other academic)
  • 15.
    Groth, Erika
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organism Biology, Physiological Botany.
    Tandre, Karolina
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organism Biology, Physiological Botany.
    Engström, Peter
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organism Biology, Physiological Botany.
    Molecular and functional evolution of the AGAMOUS subfamily MADS-domain proteinsManuscript (preprint) (Other academic)
  • 16.
    Groth, Erika
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany.
    Tandre, Karolina
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany.
    Engström, Peter
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany.
    Vergara-Silva, Francisco
    Universidad Nacional Autónoma de México.
    AGAMOUS subfamily MADS-box genes and the evolution of seed cone morphology in Cupressaceae and Taxodiaceae2011In: Evolution & Development, ISSN 1520-541X, E-ISSN 1525-142X, Vol. 13, no 2, p. 159-170Article in journal (Refereed)
    Abstract [en]

    In this comparative developmental genetics study, we test hypotheses based on fossil and morphological data on reproductive organ morphology and evolution in conifers-specifically, the ovule-bearing organ in Cupressaceae and Taxodiaceae. Genes homologous to the Arabidopsis gene AGAMOUS are expressed in ovuliferous scales of spruces (Picea) throughout development. Previous studies have shown that the AGAMOUS subfamily of MADS-box genes predates the split between angiosperms and gymnosperms, and that these genes have in part conserved functions in reproductive development among seed plants, especially in the specification of identity of the ovule-bearing organs. These data indicate that their expression in conifer families other than Pinaceae might be used as markers for organs homologous to the Pinaceae ovuliferous scale. Here we have isolated putative AGAMOUS orthologs from Cupressaceae and Taxodiaceae and analyzed their expression pattern in seed cones to test for the presence of morphological homologs of ovuliferous scales. Our results were not congruent with the hypothesis that the tooth of the Cryptomeria seed cone is homologous to the Picea ovuliferous scale. Likewise, the hypothesis that the bracts of Thujopsis and Juniperus contain fused ovuliferous scales was not supported. However, we found expression of AGAMOUS homologs in the sterile bracts of Cupressaceae seed cones at late developmental stages. This expression probably represents a novel gene function in these conifer families, since no corresponding expression has been identified in Pinaceae. Our study suggests that the evolutionary history of modern conifer cones is more diverse than previously thought.

  • 17. Kalbina, Irina
    et al.
    Wallin, Anita
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany.
    Lindh, Ingrid
    Engström, Peter
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany.
    Andersson, Sören
    Strid, Åke
    A novel chimeric MOMP antigen expressed in Escherichia coli, Arabidopsis thaliana, and Daucus carota as a potential Chlamydia trachomatis vaccine candidate2011In: Protein Expression and Purification, ISSN 1046-5928, E-ISSN 1096-0279, Vol. 80, no 2, p. 194-202Article in journal (Refereed)
    Abstract [en]

    The major outer membrane protein (MOMP) of Chlamydia trachomatis is a highly antigenic and hydrophobic transmembrane protein. Our attempts to express the full-length protein in a soluble form in Escherichia coli and in transgenic plants failed. A chimeric gene construct of C trachomatis serovar E MOMP was designed in order to increase solubility of the MOMP protein but with retained antigenicity. The designed construct was successfully expressed in E. coil, in Arabidopsis thaliana, and in Daucus carota. The chimeric MOMP expressed in and purified from E. coil was used as antigen for production of antibodies in rabbits. The anti-chimeric MOMP antibodies recognized the corresponding protein in both E. coli and in transgenic plants, as well as in inactivated C. trachomatis elementary bodies. Transgenic Arabidopsis and carrots were characterized for the number of MOMP chimeric genetic inserts and for protein expression. Stable integration of the transgene and the corresponding protein expression were demonstrated in Arabidopsis plants over at least six generations. Transgenic carrots showed a high level of expression of the chimeric MOMP - up to 3% of TSP.

  • 18.
    Müller, Christina Joy
    et al.
    Swedish Univ Agr Sci, Dept Plant Biol, Uppsala BioCtr, Ulls Vag 24E, SE-75651 Uppsala, Sweden.;Swedish Univ Agr Sci, Linnean Ctr Plant Biol Uppsala, Ulls Vag 24E, SE-75651 Uppsala, Sweden..
    Valdés, Ana Elisa
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany.
    Wang, Guodong
    Shaanxi Normal Univ, Minist Educ Med Plant Resource & Nat Pharmaceut C, Natl Engn Lab Resource Dev Endangered Chinese Cru, Key Lab,Coll Life Sci, Xian 710062, Peoples R China..
    Ramachandran, Prashanth
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany.
    Beste, Lisa
    Institutionen för växtproduktionsekologi, SLU, Uppsala.
    Uddenberg, Daniel
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany.
    Carlsbecker, Annelie
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany.
    PHABULOSA Mediates an Auxin Signaling Loop to Regulate Vascular Patterning in Arabidopsis2016In: Plant Physiology, ISSN 0032-0889, E-ISSN 1532-2548, Vol. 170, no 2, p. 956-970Article in journal (Refereed)
    Abstract [en]

    Plant vascular tissues, xylem and phloem, differentiate in distinct patterns from procambial cells as an integral transport system for water, sugars, and signaling molecules. Procambium formation is promoted by high auxin levels activating class III homeodomain leucine zipper (HD-ZIP III) transcription factors (TFs). In the root of Arabidopsis (Arabidopsis thaliana), HD-ZIP III TFs dose-dependently govern the patterning of the xylem axis, with higher levels promoting metaxylem cell identity in the central axis and lower levels promoting protoxylem at its flanks. It is unclear, however, by what mechanisms the HD-ZIP III TFs control xylem axis patterning. Here, we present data suggesting that an important mechanism is their ability to moderate the auxin response. We found that changes in HD-ZIP III TF levels affect the expression of genes encoding core auxin response molecules. We show that one of the HD-ZIP III TFs, PHABULOSA, directly binds the promoter of both MONOPTEROS (MP)/AUXIN RESPONSE FACTOR5, a key factor in vascular formation, and IAA20, encoding an auxin/indole acetic acid protein that is stable in the presence of auxin and able to interact with and repress MP activity. The double mutant of IAA20 and its closest homolog IAA30 forms ectopic protoxylem, while overexpression of IAA30 causes discontinuous protoxylem and occasional ectopic metaxylem, similar to a weak loss-of-function mp mutant. Our results provide evidence that HD-ZIP III TFs directly affect the auxin response and mediate a feed-forward loop formed by MP and IAA20 that may focus and stabilize the auxin response during vascular patterning and the differentiation of xylem cell types.

  • 19.
    Orizaola, German
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Valdés, Ana Elisa
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany.
    Free the tweet at scientific conferences2015In: Science, ISSN 0036-8075, E-ISSN 1095-9203, Vol. 350, no 6257, p. 170-U149Article in journal (Refereed)
  • 20.
    Orizaola, Germán
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Valdés, Ana Elisa
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany.
    Redes Sociales para el Desarrollo Científico2015In: The Information and Scientific News Service (SINC)Article in journal (Other (popular science, discussion, etc.))
  • 21.
    Ramachandran, Prashanth
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany.
    Carlsbecker, Annelie
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany.
    Etchells, J. Peter
    Univ Durham, Dept Biosci, South Rd, Durham DH1 3LE, England..
    Class III HD- ZIPs govern vascular cell fate: an HD view on patterning and differentiation2017In: Journal of Experimental Botany, ISSN 0022-0957, E-ISSN 1460-2431, Vol. 68, no 1, p. 55-69Article, review/survey (Refereed)
    Abstract [en]

    Plant vasculature is required for the transport of water and solutes throughout the plant body. It is constituted of xylem, specialized for transport of water, and phloem, that transports photosynthates. These two differentiated tissues are specified early in development and arise from divisions in the procambium, which is the vascular meristem during primary growth. During secondary growth, the xylem and phloem are further expanded via differentiation of cells derived from divisions in the cambium. Almost all of the developmental fate decisions in this process, including vascular specification, patterning, and differentiation, are regulated by transcription factors belonging to the class III homeodomain-leucine zipper (HD-ZIP III) family. This review draws together the literature describing the roles that these genes play in vascular development, looking at how HD-ZIP IIIs are regulated, and how they in turn influence other regulators of vascular development. Themes covered vary, from interactions between HD-ZIP IIIs and auxin, cytokinin, and brassinosteroids, to the requirement for exquisite spatial and temporal regulation of HD-ZIP III expression through miRNA-mediated post-transcriptional regulation, and interactions with other transcription factors. The literature described places the HD-ZIP III family at the centre of a complex network required for initiating and maintaining plant vascular tissues.

  • 22.
    Ramachandran, Prashanth
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany. Linnean Ctr Plant Biol, Ullsv 24E, SE-75651 Uppsala, Sweden.
    Wang, Guodong
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany. Linnean Ctr Plant Biol, Ullsv 24E, SE-75651 Uppsala, Sweden.
    Augstein, Frauke
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany. Linnean Ctr Plant Biol, Ullsv 24E, SE-75651 Uppsala, Sweden.
    de Vries, Jan
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany. Linnean Ctr Plant Biol, Ullsv 24E, SE-75651 Uppsala, Sweden, Canada..
    Carlsbecker, Annelie
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany. Linnean Ctr Plant Biol, Ullsv 24E, SE-75651 Uppsala, Sweden.
    Continuous root xylem formation and vascular acclimation to water deficit involves endodermal ABA signalling via miR1652018In: Development, ISSN 0950-1991, E-ISSN 1477-9129, Vol. 145, no 3, article id dev159202Article in journal (Refereed)
    Abstract [en]

    The plant root xylem comprises a specialized tissue for water distribution to the shoot. Despite its importance, its potential morphological plasticity in response to environmental conditions such as limited water availability has not been thoroughly studied. Here, we identify a role for the phytohormone abscisic acid (ABA) for proper xylem development and describe how ABA signalling-mediated effects on core developmental regulators are employed to alter xylem morphology under limited water availability in Arabidopsis. Plants with impaired ABA biosynthesis and reduced ABA signalling in the cell layer surrounding the vasculature displayed defects in xylem continuity, suggesting that non-cell autonomous ABA signalling is required for proper xylem development. Conversely, upon external ABA application or under limited water availability, extra xylem strands were formed. The observed xylem developmental alterations were dependent on adequate endodermal ABA signalling, which activated MIR165A. This resulted in increased miR165 levels that repress class III HD-ZIP transcription factors in the stele. We conclude that a pathway known to control core developmental features is employed as a means of modifying plant xylem morphology under conditions of environmental stress.

  • 23.
    Reza, Salim H.
    et al.
    Swedish Univ Agr Sci, Linnean Ctr Plant Biol, Uppsala BioCtr, Dept Plant Biol, Uppsala, Sweden.;Swedish Univ Agr Sci, Linnean Ctr Plant Biol, Uppsala BioCtr, Dept Mol Sci, Uppsala, Sweden..
    Delhomme, Nicolas
    Swedish Univ Agr Sci, Dept Forest Genet & Plant Physiol, Umea Plant Sci Ctr, Umea, Sweden..
    Street, Nathaniel R.
    Umea Univ, Dept Plant Physiol, Umea Plant Sci Ctr, Umea, Sweden..
    Ramachandran, Prashanth
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany.
    Dalman, Kerstin
    Swedish Univ Agr Sci, Linnean Ctr Plant Biol, Uppsala BioCtr, Dept Mol Sci, Uppsala, Sweden..
    Nilsson, Ove
    Swedish Univ Agr Sci, Dept Forest Genet & Plant Physiol, Umea Plant Sci Ctr, Umea, Sweden..
    Minina, Elena A.
    Swedish Univ Agr Sci, Linnean Ctr Plant Biol, Uppsala BioCtr, Dept Mol Sci, Uppsala, Sweden..
    Bozhkov, Peter V.
    Swedish Univ Agr Sci, Linnean Ctr Plant Biol, Uppsala BioCtr, Dept Mol Sci, Uppsala, Sweden..
    Transcriptome analysis of embryonic domains in Norway spruce reveals potential regulators of suspensor cell death2018In: PLoS ONE, ISSN 1932-6203, E-ISSN 1932-6203, Vol. 13, no 3, article id e0192945Article in journal (Refereed)
    Abstract [en]

    The terminal differentiation and elimination of the embryo-suspensor is the earliest manifestation of programmed cell death (PCD) during plant ontogenesis. Molecular regulation of suspensor PCD remains poorly understood. Norway spruce (Picea abies) embryos provide a powerful model for studying embryo development because of their large size, sequenced genome, and the possibility to obtain a large number of embryos at a specific developmental stage through somatic embryogenesis. Here, we have carried out global gene expression analysis of the Norway spruce embryo-suspensor versus embryonal mass (a gymnosperm analogue of embryo proper) using RNA sequencing. We have identified that suspensors have enhanced expression of the NAC domain-containing transcription factors, XND1 and ANAC075, previously shown to be involved in the initiation of developmental PCD in Arabidiopsis. The analysis has also revealed enhanced expression of Norway spruce homologues of the known executioners of both developmental and stress-induced cell deaths, such as metacaspase 9 (MC9), cysteine endopeptidase-1 (CEP1) and ribonuclease 3 (RNS3). Interestingly, a spruce homologue of bax inhibitor-1 (PaBI-1, for Picea abies BI-1), an evolutionarily conserved cell death suppressor, was likewise up-regulated in the embryosuspensor. Since Arabidopsis BI-1 so far has been implicated only in the endoplasmic reticulum (ER)-stress induced cell death, we investigated its role in embryogenesis and suspensor PCD using RNA interference (RNAi). We have found that PaBI-1-deficient lines formed a large number of abnormal embryos with suppressed suspensor elongation and disturbed polarity. Cytochemical staining of suspensor cells has revealed that PaBI-1 deficiency suppresses vacuolar cell death and induces necrotic type of cell death previously shown to compromise embryo development. This study demonstrates that a large number of cell-death components are conserved between angiosperms and gymnosperms and establishes a new role for BI-1 in the progression of vacuolar cell death.

  • 24.
    Rizzardi, Kristina
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany.
    Epigenetic Regulation of Light and Hormonal Signaling in Arabidopsis thaliana2011Doctoral thesis, comprehensive summary (Other academic)
    Abstract [en]

    Plants are stationary and need to adapt to the environment they live in. Integration of environmental cues, such as changes in light and temperature, can occur either directly or through the action of hormones. Hormone and light signaling leads to rapid changes in gene expression, and eventually changes in protein levels. In this thesis I have studied how the epigenetic regulator TERMINAL FLOWER2 (TFL2) is involved in light and hormonal signaling in the model organism Arabidopsis thaliana (thale cress). TFL2 is the only Arabidopsis homologue of HETEROCHROMATIN PROTEIN1 (HP1). HP1 proteins have been shown to be involved in repressing gene expression by maintaining the tight structure of heterochromatin or by forming a heterochromatin like structure in euchromatic regions. Unlike metazoan HP1 which can be localized both to eu- and heterochromatin, TFL2 is uniquely localized to euchromatin.

    tfl2 mutants have reduced levels of free auxin and a reduced rate of auxin biosynthesis. TFL2 binds to and promotes spatial and temporal expression of the genes belonging to the YUCCA gene family, which are believed to regulate a rate limiting step in the auxin biosynthesis pathway. Further, TFL2 binds to a subset of Aux/IAA proteins to repress auxin regulated genes involved in ovule and carpel development. In a similar way, TFL2 is also involved in repressing two jasmonate responsive genes, VEGETATIVE STORAGE PROTEIN1 and 2. This TFL2 regulated repression might occur through the interaction with the jasmonate responsive protein JAZ6.

    In light signaling TFL2 is involved in repressing both phytochrome A and B signaling as the response to red and far red light is enhanced in tfl2 mutants. The shade avoidance response and chloroplast biogenesis are also regulated by TFL2 as the hypocotyls of tfl2 are not able to elongate as wt in shade conditions and greening is delayed upon de-etiolation of tfl2 seedlings.

    This work shows that TFL2 has a repressive function in auxin, jasmonate and light signaling and for the first time we show that TFL2 is directly involved in promoting gene expression.

    List of papers
    1. TFL2/LHP1 is involved in auxin biosynthesis through positive regulation of YUCCA genes
    Open this publication in new window or tab >>TFL2/LHP1 is involved in auxin biosynthesis through positive regulation of YUCCA genes
    Show others...
    2011 (English)In: The Plant Journal, ISSN 0960-7412, E-ISSN 1365-313X, Vol. 65, no 6, p. 897-906Article in journal (Refereed) Published
    Abstract [en]

    TERMINAL FLOWER2 (TFL2) is the plant homologue of metazoan HETEROCHROMATIN PROTEIN1 (HP1) protein family. It is known that, unlike most HP1 proteins, TFL2 does not primarily localize to heterochromatin; instead it functions in regulation of specific genes in euchromatic regions. We show that the tfl2 mutant has a lower rate of auxin biosynthesis, resulting in low levels of auxin. In line with this, tfl2 mutants have lower levels of expression of auxin response genes and retain an auxin response. The reduced rate of auxin biosynthesis in tfl2 is correlated to the down-regulation of specific genes in the tryptophan-dependent auxin biosynthesis pathway, a sub-set of the YUCCA genes. In vivo, TFL2 is targeted to a number of the YUCCA genes in an auxin-dependent fashion revealing a role of TFL2 in auxin regulation, probably as a component of protein complexes affecting transcriptional control.

    Keywords
    TERMINAL FLOWER2/LIKE HETEROCHROMATIN PROTEIN1, Aux/IAA, auxin response, auxin biosynthesis, YUCCA, epigenetic
    National Category
    Biological Sciences
    Identifiers
    urn:nbn:se:uu:diva-150719 (URN)10.1111/j.1365-313X.2010.04470.x (DOI)000288449700005 ()21251106 (PubMedID)
    Available from: 2011-04-05 Created: 2011-04-05 Last updated: 2017-12-11Bibliographically approved
    2. TERMINAL FLOWER2 is involved in auxin signaling and acts together with IAA6 to repress SHATTERPROOF1 outside its functional domains.
    Open this publication in new window or tab >>TERMINAL FLOWER2 is involved in auxin signaling and acts together with IAA6 to repress SHATTERPROOF1 outside its functional domains.
    (English)Article in journal (Refereed) Submitted
    Identifiers
    urn:nbn:se:uu:diva-151805 (URN)
    Available from: 2011-04-18 Created: 2011-04-18 Last updated: 2011-07-01
    3. TERMINAL FLOWER2, an epigenetic repressor involved jasmonate signaling.
    Open this publication in new window or tab >>TERMINAL FLOWER2, an epigenetic repressor involved jasmonate signaling.
    (English)Article in journal (Refereed) Submitted
    Identifiers
    urn:nbn:se:uu:diva-151806 (URN)
    Available from: 2011-04-18 Created: 2011-04-18 Last updated: 2011-07-01
    4. Arabidopsis thaliana TERMINAL FLOWER2 is involved in light controlled signaling during seedling photomorphogenesis
    Open this publication in new window or tab >>Arabidopsis thaliana TERMINAL FLOWER2 is involved in light controlled signaling during seedling photomorphogenesis
    Show others...
    2012 (English)In: Plant, Cell and Environment, ISSN 0140-7791, E-ISSN 1365-3040, Vol. 35, no 6, p. 1013-1025Article in journal (Refereed) Published
    Abstract [en]

    Plants respond to changes in the environment by altering their growth pattern. Light is one of the most important environmental cues and affects plants throughout the life cycle. It is perceived by photoreceptors such as phytochromes that absorb light of red and far-red wavelengths and control, for example, seedling de-etiolation, chlorophyll biosynthesis and shade avoidance response. We report that the terminal flower2 (tfl2) mutant, carrying a mutation in the Arabidopsis thaliana HETEROCHROMATIN PROTEIN1 homolog, functions in negative regulation of phytochrome dependent light signalling. tfl2 shows defects in both hypocotyl elongation and shade avoidance response. Double mutant analysis indicates that mutants of the red/far-red light absorbing phytochrome family of plant photoreceptors, phyA and phyB, are epistatic to tfl2 in far-red and red light, respectively. An overlap between genes regulated by light and by auxin has earlier been reported and, in tfl2 plants light-dependent auxin-regulated genes are misexpressed. Further, we show that TFL2 binds to IAA5 and IAA19 suggesting that TFL2 might be involved in regulation of phytochrome-mediated light responses through auxin action.

    Keywords
    auxin, LIKE HETEROCHROMATIN PROTEIN1, phytochrome, shade avoidance response
    National Category
    Biological Sciences
    Identifiers
    urn:nbn:se:uu:diva-151807 (URN)10.1111/j.1365-3040.2011.02468.x (DOI)000303052500001 ()
    Note

    Valdés Ana Elisa and Rizzardi Kristina have contributed equally to this work

    Available from: 2011-04-18 Created: 2011-04-18 Last updated: 2017-12-11Bibliographically approved
  • 25.
    Rizzardi, Kristina
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany.
    Landberg, Katarina
    Nilsson, Lars
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany.
    Ljung, Karin
    Sundås-Larsson, Annika
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany.
    TFL2/LHP1 is involved in auxin biosynthesis through positive regulation of YUCCA genes2011In: The Plant Journal, ISSN 0960-7412, E-ISSN 1365-313X, Vol. 65, no 6, p. 897-906Article in journal (Refereed)
    Abstract [en]

    TERMINAL FLOWER2 (TFL2) is the plant homologue of metazoan HETEROCHROMATIN PROTEIN1 (HP1) protein family. It is known that, unlike most HP1 proteins, TFL2 does not primarily localize to heterochromatin; instead it functions in regulation of specific genes in euchromatic regions. We show that the tfl2 mutant has a lower rate of auxin biosynthesis, resulting in low levels of auxin. In line with this, tfl2 mutants have lower levels of expression of auxin response genes and retain an auxin response. The reduced rate of auxin biosynthesis in tfl2 is correlated to the down-regulation of specific genes in the tryptophan-dependent auxin biosynthesis pathway, a sub-set of the YUCCA genes. In vivo, TFL2 is targeted to a number of the YUCCA genes in an auxin-dependent fashion revealing a role of TFL2 in auxin regulation, probably as a component of protein complexes affecting transcriptional control.

  • 26.
    Rizzardi, Kristina
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany.
    Landberg, Katarina
    SLU, Department of Plant Biology and forest Genetics.
    Sundås-Larsson, Annika
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany.
    TERMINAL FLOWER2, an epigenetic repressor involved jasmonate signaling.Article in journal (Refereed)
  • 27.
    Rizzardi, Kristina
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany.
    Landberg, Katarina
    SLU, Department of Plant Biology and forest Genetics.
    Sundås-Larsson, Annika
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany.
    TERMINAL FLOWER2 is involved in auxin signaling and acts together with IAA6 to repress SHATTERPROOF1 outside its functional domains.Article in journal (Refereed)
  • 28.
    Roberts, Christina
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany.
    Help, Hanna
    Institute of Biotecnology, University of Helsinki, Finland.
    Helariutta, Ykä
    Institute of Biotecnology, University of Helsinki, Finland.
    Carlsbecker, Annelie
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany.
    Class III HD-ZIP Transcription Factors Regulate Auxin Signalling to Pattern Arabidopsis Root VasculatureManuscript (preprint) (Other academic)
  • 29.
    Roberts, Christina Joy
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany.
    Cell-to-Cell Signalling in Arabidopsis Root Development2012Doctoral thesis, comprehensive summary (Other academic)
    Abstract [en]

    Development in multicellular organisms requires a strict balance between cell division and differentiation. The simple architecture of the Arabidopsis thaliana root makes it an ideal model for studying molecular mechanisms controlling both the transition from cell division to cell differentiation and cell fate determination. The class III Homeodomain-Leucine Zipper (HD-ZIP III) transcription factors (TFs) are well known developmental regulators, controlling important aspects of embryogenesis, shoot meristem activity, leaf polarity and vascular patterning. The HD-ZIP III TFs are under post-transcriptional control of microRNA165 (miR165) and miR166. In this thesis, I present a cell-to-cell signalling pathway underlying root vascular patterning and describe signaling pathways downstream of the HD-ZIP III TFs in their control of root development. The TF SHORTROOT (SHR), moves from the vascular stele cells to the surrounding endodermal cell layer. We show that SHR acts here to transcriptionally activate MIR165A and MIR166B, and the miR165/6 produced in the endodermis act non-cell autonomously to post-transcriptionally restrict HD-ZIP III mRNA levels in the peripheral stele. The resulting graded HD-ZIP III activity domain in the radial stele dose-dependently determines vascular cell type; high levels of HD-ZIP III in the central stele result in metaxylem formation while lower levels in the peripheral stele result in protoxylem. We provide evidence that the HD-ZIP III factors act as de novo xylem specifiers, because the quintuple mutant lacking all five HD-ZIP III genes forms no xylem. Furthermore, reducing the plasmodesmatal aperture through callose accumulation inhibits the bi-directional mobility of both signalling molecules, providing evidence that both SHR and miR165/6 move cell-to-cell via plasmodesmata to control root development.

    I present downstream components of the miR165/HD-ZIP III TFs in the root meristem, identified through a time-course induction of miR165 coupled to transcriptome analyses. This experiment revealed novel roles for HD-ZIP III TFs in vascular patterning and meristem size control. I show that HD-ZIP III directed repression of auxin hormone signalling in the xylem axis is essential for proper xylem differentiation. Furthermore, I provide data to show that they also control the balance of reactive oxygen species in the root meristem, thereby directing meristem size and ultimately controlling root growth.

    List of papers
    1. Cell signalling by microRNA165/6 directs gene dose-dependent root cell fate
    Open this publication in new window or tab >>Cell signalling by microRNA165/6 directs gene dose-dependent root cell fate
    Show others...
    2010 (English)In: Nature, ISSN 0028-0836, E-ISSN 1476-4687, Vol. 465, no 7296, p. 316-321Article in journal (Refereed) Published
    Abstract [en]

    A key question in developmental biology is how cells exchange positional information for proper patterning during organ development. In plant roots the radial tissue organization is highly conserved with a central vascular cylinder in which two water conducting cell types, protoxylem and metaxylem, are patterned centripetally. We show that this patterning occurs through crosstalk between the vascular cylinder and the surrounding endodermis mediated by cell-to-cell movement of a transcription factor in one direction and microRNAs in the other. SHORT ROOT, produced in the vascular cylinder, moves into the endodermis to activate SCARECROW. Together these transcription factors activate MIR165a and MIR166b. Endodermally produced microRNA165/6 then acts to degrade its target mRNAs encoding class III homeodomain-leucine zipper transcription factors in the endodermis and stele periphery. The resulting differential distribution of target mRNA in the vascular cylinder determines xylem cell types in a dosage-dependent manner.

    National Category
    Biological Sciences
    Identifiers
    urn:nbn:se:uu:diva-136559 (URN)10.1038/nature08977 (DOI)000277829200033 ()20410882 (PubMedID)
    Available from: 2010-12-14 Created: 2010-12-13 Last updated: 2017-12-11Bibliographically approved
    2. Callose Biosynthesis Regulates Symplastic Trafficking during Root Development
    Open this publication in new window or tab >>Callose Biosynthesis Regulates Symplastic Trafficking during Root Development
    Show others...
    2011 (English)In: Developmental Cell, ISSN 1534-5807, E-ISSN 1878-1551, Vol. 21, no 6, p. 1144-1155Article in journal (Refereed) Published
    Abstract [en]

    Plant cells are connected through plasmodesmata (PD), membrane-lined channels that allow symplastic movement of molecules between cells. However, little is known about the role of PD-mediated signaling during plant morphogenesis. Here, we describe an Arabidopsis gene, CALS3/GSL12. Gain-of-function mutations in CALS3 result in increased accumulation of callose (beta-1,3-glucan) at the PD, a decrease in PD aperture, defects in root development, and reduced intercellular trafficking. Enhancement of CALS3 expression during phloem development suppressed loss-of-function mutations in the phloem abundant callose synthase, CALS7 indicating that CALS3 is a bona fide callose synthase. CALS3 alleles allowed us to spatially and temporally control the PD aperture between plant tissues. Using this tool, we are able to show that movement of the transcription factor SHORT-ROOT and microRNA1 65 between the stele and the endodermis is PD dependent. Taken together, we conclude that regulated callose biosynthesis at PD is essential for cell signaling.

    National Category
    Natural Sciences Medical and Health Sciences
    Identifiers
    urn:nbn:se:uu:diva-167203 (URN)10.1016/j.devcel.2011.10.006 (DOI)000298215200018 ()
    Available from: 2012-01-23 Created: 2012-01-23 Last updated: 2017-12-08Bibliographically approved
    3. Class III HD-ZIP Transcription Factors Determine Root Meristem Size by Controlling Reactive Oxygen Species Levels
    Open this publication in new window or tab >>Class III HD-ZIP Transcription Factors Determine Root Meristem Size by Controlling Reactive Oxygen Species Levels
    (English)Manuscript (preprint) (Other academic)
    National Category
    Botany
    Identifiers
    urn:nbn:se:uu:diva-181188 (URN)
    Available from: 2012-10-03 Created: 2012-09-18 Last updated: 2016-04-25
    4. Class III HD-ZIP Transcription Factors Regulate Auxin Signalling to Pattern Arabidopsis Root Vasculature
    Open this publication in new window or tab >>Class III HD-ZIP Transcription Factors Regulate Auxin Signalling to Pattern Arabidopsis Root Vasculature
    (English)Manuscript (preprint) (Other academic)
    National Category
    Botany
    Identifiers
    urn:nbn:se:uu:diva-181189 (URN)
    Available from: 2012-10-03 Created: 2012-09-18 Last updated: 2016-04-25
  • 30.
    Roberts, Christina Joy
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany.
    Valdés, Ana Elisa
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany.
    Carlsbecker, Annelie
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany.
    Class III HD-ZIP transcription factors control root growth and vascular patterning2013Conference paper (Other academic)
  • 31.
    Roberts, Christina Joy
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany.
    Valdés, Ana Elisa
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany.
    Carlsbecker, Annelie
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology.
    Mechanisms of root growth and vascular patterning regulation by the class III HD-ZIP transcription factors2013Conference paper (Other academic)
  • 32.
    Roberts, Christina
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany.
    Valdés, Ana Elisa
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany.
    Carlsbecker, Annelie
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany.
    Class III HD-Zip transcription factors control root growth and vascular patterning2013Conference paper (Other academic)
  • 33.
    Roberts, Christina
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany.
    Valdés, Ana Elisa
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany.
    Carlsbecker, Annelie
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany.
    Class III HD-ZIP Transcription Factors Determine Root Meristem Size by Controlling Reactive Oxygen Species LevelsManuscript (preprint) (Other academic)
  • 34.
    Roberts, Christina
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany.
    Valdés, Ana Elisa
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany.
    Carlsbecker, Annelie
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany.
    HD-Zip Class III Transcription factors control root growth and vascular patterning2012Conference paper (Other academic)
    Abstract [en]

    Plants take up water and mineral nutrients through their roots, and this is then distributed throughout the plant via the vascular tissues. Hence, root growth and vascular patterning and differentiation are likely intimately connected to optimize water and nutrient uptake. Mutants defective in the developmental control regulators encoded by Class III homeodomain leucine zipper (HD-ZIP III) genes display alterations both in root growth rates and in vascular patterning. In the wild-type root, the water conducting strands are invariantly patterned such that protoxylem, with spiral or annular secondary walls, occupies peripheral positions in the vascular stele, and metaxylem, characterized by reticulate or pitted secondary walls, are found in central positions. This pattern is altered by mutations in the HD-ZIP III genes: the phb-7d gain-of-function mutant has metaxylem also in protoxylem position, while the athb8 cna phb phv quadruple loss-of-function mutant develops protoxylem in both central and peripheral positions. We have recently shown that the miR165/166 targeting the HD-ZIP III genes moves from the surrounding endodermal cell layer to control the levels of the HD-ZIP III factors in the stele, and that xylem cell fate is dependent on HD-ZIP III levels; high levels specify metaxylem and low levels specify protoxylem (Carlsbecker et al. Nature, 465(7296):316-21, 2010). Similarly, the levels of HD-ZIP III factors appear to determine both root growth rate and meristem size. While phb-7d has a short root and small root apical meristem, the athb8 cna phb phv quadruple mutant has a long root and large apical meristem. To determine what genes are under the control of the HD-ZIP III transcription factors in the root meristem, we have conducted analyses of transcriptome changes upon either inducing a gain-of-function allele of PHB or inducing miR165 to reduce HD-ZIP III levels. Our analyses suggest that the HD-ZIP III transcription factors act upstream of secondary cell wall and programmed cell death control genes, consistent with the observed xylem phenotypes, but are also upstream of a genetic pathway controlling meristem size and growth rate. Hence, the HD-ZIP III transcription factors may act to integrate root growth control and vascular patterning.

  • 35.
    Tandre, Karolina
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organism Biology, Physiological Botany.
    Groth, Erika
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organism Biology, Physiological Botany.
    Liu, Shuoran
    Engström, Peter
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organism Biology, Physiological Botany.
    Identification and characterization of basal AGAMOUS subfamily MADS-box genes from Norway spruce (Picea abies); implications for the evolution of AGAMOUS subfamily genes in seed plantsManuscript (preprint) (Other academic)
  • 36.
    Uddenberg, Daniel
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany. Swedish Univ Agr Sci, Dept Plant Biol, POB 7080, S-75007 Uppsala, Sweden.;Swedish Univ Agr Sci, Uppsala BioCtr, Linnean Ctr Plant Biol, POB 7080, S-75007 Uppsala, Sweden..
    Abrahamsson, Malin
    Swedish Univ Agr Sci, Dept Plant Biol, POB 7080, S-75007 Uppsala, Sweden.;Swedish Univ Agr Sci, Uppsala BioCtr, Linnean Ctr Plant Biol, POB 7080, S-75007 Uppsala, Sweden..
    von Arnold, Sara
    Swedish Univ Agr Sci, Dept Plant Biol, POB 7080, S-75007 Uppsala, Sweden.;Swedish Univ Agr Sci, Uppsala BioCtr, Linnean Ctr Plant Biol, POB 7080, S-75007 Uppsala, Sweden..
    Overexpression of PaHAP3A stimulates differentiation of ectopic embryos from maturing somatic embryos of Norway spruce2016In: Tree Genetics & Genomes, ISSN 1614-2942, E-ISSN 1614-2950, Vol. 12, no 2, article id 18Article in journal (Refereed)
    Abstract [en]

    Somatic embryogenesis can be used for large-scale propagation of plants. In most conifers, it is only possible to establish embryogenic cultures from zygotic embryos or young seedlings. There is, however, a great interest to propagate selected trees with valuable traits via somatic embryos. To be able to establish embryogenic cultures from adult tissues, more knowledge about the molecular regulation of totipotency and embryogenic potential is needed. In Arabidopsis (Arabidopsis thaliana), LEAFY COTYLEDON1 (LEC1) is required for somatic embryogenesis, and overexpression of LEC1 can stimulate the formation of embryo-like structures from vegetative tissues. We have previously characterized a conifer LEC1-type gene, PaHAP3A, which is preferentially active during embryo development in Norway spruce (Picea abies). In this work, we show, by using histochemical GUS assays, that PaHAP3A is expressed in germinated embryos at presumptive sites from which embryogenic tissue differentiate during initiation of embryogenic cultures. Furthermore, we have overexpressed PaHAP3A, using both constitutive and inducible promoters, in order to elucidate whether elevated transcript levels of PaHAP3A are sufficient to induce embryonic properties after germination. In contrast to its angiosperm counterpart, PaHAP3A does not stimulate embryonic features in vegetative tissues. However, overexpression of PaHAP3A during the maturation stage leads to the differentiation of ectopic embryos from maturing somatic embryos. Our results not only indicate at least partial conservation between the conifer and angiosperm LEC1-type genes but also suggest that PaHAP3A is dependent of the cellular status to confer its presumptive role as an important factor influencing the competence of the tissue to initiate somatic embryos.

  • 37. Uddenberg, Daniel
    et al.
    Valladares, Silvia
    Abrahamsson, Malin
    Sundström, Jens Fredrik
    Sundås-Larsson, Annika
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany.
    von Arnold, Sara
    Embryogenic potential and expression of embryogenesis-related genes in conifers are affected by treatment with a histone deacetylase inhibitor2011In: Planta, ISSN 0032-0935, E-ISSN 1432-2048, Vol. 234, no 3, p. 527-539Article in journal (Refereed)
    Abstract [en]

    Somatic embryogenesis is used for vegetative propagation of conifers. Embryogenic cultures can be established from zygotic embryos; however, the embryogenic potential decreases during germination. In Arabidopsis, LEAFY COTYLEDON (LEC) genes are expressed during the embryonic stage, and must be repressed to allow germination. Treatment with the histone deacetylase inhibitor trichostatin A (TSA) causes de-repression of LEC genes. ABSCISIC ACID3 (ABI3) and its Zea mays ortholog VIVIPAROUS1 (VP1) act together with the LEC genes to promote embryo maturation. In this study, we have asked the question whether TSA treatment in a conifer affects the embryogenic potential and the expression of embryogenesis-related genes. We isolated two conifer LEC1-type HAP3 genes, HAP3A and HAP3B, from Picea abies and Pinus sylvestris. A comparative phylogenetic analysis of plant HAP3 genes suggests that HAP3A and HAP3B are paralogous genes originating from a duplication event in the conifer lineage. The expression of HAP3A is high, in both somatic and zygotic embryos, during early embryo development, but decreases during late embryogeny. In contrast, the expression of VP1 is initially low but increases during late embryogeny. After exposure to TSA, germinating somatic embryos of P. abies maintain the competence to differentiate embryogenic tissue, and simultaneously the germination progression is partially inhibited. Furthermore, when embryogenic cultures of P. abies are exposed to TSA during embryo maturation, the maturation process is arrested and the expression levels of PaHAP3A and PaVP1 are maintained, suggesting a possible link between chromatin structure and expression of embryogenesis-related genes in conifers.

  • 38. Ursache, Robertas
    et al.
    Miyashima, Shunsuke
    Chen, Qingguo
    Vaten, Anne
    Nakajima, Keiji
    Carlsbecker, Annelie
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany.
    Zhao, Yunde
    Helariutta, Yka
    Dettmer, Jan
    Tryptophan-dependent auxin biosynthesis is required for HD-ZIP III-mediated xylem patterning2014In: Development, ISSN 0950-1991, E-ISSN 1477-9129, Vol. 141, no 6, p. 1250-1260Article in journal (Refereed)
    Abstract [en]

    The development and growth of higher plants is highly dependent on the conduction of water and minerals throughout the plant by xylem vessels. In Arabidopsis roots the xylem is organized as an axis of cell files with two distinct cell fates: the central metaxylem and the peripheral protoxylem. During vascular development, high and low expression levels of the class III HD-ZIP transcription factors promote metaxylem and protoxylem identities, respectively. Protoxylem specification is determined by both mobile, ground tissue-emanating miRNA165/6 species, which downregulate, and auxin concentrated by polar transport, which promotes HD-ZIP III expression. However, the factors promoting high HD-ZIP III expression for metaxylem identity have remained elusive. We show here that auxin biosynthesis promotes HD-ZIP III expression and metaxylem specification. Several auxin biosynthesis genes are expressed in the outer layers surrounding the vascular tissue in Arabidopsis root and downregulation of HD-ZIP III expression accompanied by specific defects in metaxylem development is seen in auxin biosynthesis mutants, such as trp2-12, wei8 tar2 or a quintuple yucca mutant, and in plants treated with L-kynurenine, a pharmacological inhibitor of auxin biosynthesis. Some of the patterning defects can be suppressed by synthetically elevated HD-ZIP III expression. Taken together, our results indicate that polar auxin transport, which was earlier shown to be required for protoxylem formation, is not sufficient to establish a proper xylem axis but that root-based auxin biosynthesis is additionally required.

  • 39.
    Valdés, Ana Elisa
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany.
    Forced adaptation: plant proteins to fight climate change2015In: Frontiers in Plant Science, ISSN 1664-462X, E-ISSN 1664-462X, Vol. 5, article id 762Article in journal (Refereed)
  • 40.
    Valdés, Ana Elisa
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany.
    Herud, Ole
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany.
    Engström, Peter
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany.
    HD-Zip class I genes as components of ABA and drought signalling system in Arabidopsis thaliana2008Conference paper (Other academic)
  • 41.
    Valdés, Ana Elisa
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany.
    Irar, Sami
    Majadad, Juan P.
    Rodriguez, Ana
    Fernandez, Belen
    Pages, Montserrat
    Drought tolerance acquisition in Eucalyptus globulus (Labill.): A research on plant morphology, physiology and proteomics2013In: Journal of Proteomics, ISSN 1874-3919, E-ISSN 1876-7737, Vol. 79, p. 263-276Article in journal (Refereed)
    Abstract [en]

    Plants perceiving drought stress activate multiple responses to synchronise developmental and molecular activities aimed at improving survival. In this study we attained a multidisciplinary approach to examine the interplay among plant morphology, physiology and proteomics for understanding the mechanisms underlying the adaptive response to drought stress. The stress-related phenotype, the differential expression of putative members of the LEA family of proteins, the seed proteomic profile, and the endogenous content of free and conjugated abscisic acid (ABA and ABAGE) were analysed in two Eucalyptus globulus provenances with contrasting drought tolerance. Differences in morphology were noticeable, drought-tolerant genotypes displaying smaller seeds with higher desiccation in the mature state and a more developed root system that was not reduced under water stress treatments. From physiological and molecular points of view, the endogenous contents of ABA and ABAGE were also higher in the tolerant provenance, as well as the accumulation of proteins involved in abiotic stress tolerance processes. In addition, evidence of two immunologically-related proteins to the maize RAB17 and RAB28 proteins is first reported in Eucalyptus, showing similarities between species. Our results show that E. globulus displays simultaneous adjustments for acquiring drought tolerance that are expressed at physiological, developmental and molecular levels.

  • 42.
    Valdés, Ana Elisa
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany.
    Majada, Juan P
    SERIDA, Spain.
    Rodriguez, Ana
    University of Oviedo, Spain.
    Fernandez, Belen
    University of Oviedo, Spain.
    Pagés, Montserrat
    CSIC, Spain.
    Irar, Sami
    CSIC, Spain.
    A multidisciplinary approach to drought tolerance acquisition in Eucalyptus globulus (Labill.): plant morphology, physiology and proteomics.2012Conference paper (Other academic)
  • 43.
    Valdés, Ana Elisa
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany.
    Rizzardi, Kristina
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany.
    Johannesson, Henrik
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany.
    Para, Alessia
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany.
    Sundås-Larsson, Annika
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany.
    Landberg, Katarina
    SLU, Department of Plant Biology and forest Genetics.
    Arabidopsis thaliana TERMINAL FLOWER2 is involved in light controlled signaling during seedling photomorphogenesis2012In: Plant, Cell and Environment, ISSN 0140-7791, E-ISSN 1365-3040, Vol. 35, no 6, p. 1013-1025Article in journal (Refereed)
    Abstract [en]

    Plants respond to changes in the environment by altering their growth pattern. Light is one of the most important environmental cues and affects plants throughout the life cycle. It is perceived by photoreceptors such as phytochromes that absorb light of red and far-red wavelengths and control, for example, seedling de-etiolation, chlorophyll biosynthesis and shade avoidance response. We report that the terminal flower2 (tfl2) mutant, carrying a mutation in the Arabidopsis thaliana HETEROCHROMATIN PROTEIN1 homolog, functions in negative regulation of phytochrome dependent light signalling. tfl2 shows defects in both hypocotyl elongation and shade avoidance response. Double mutant analysis indicates that mutants of the red/far-red light absorbing phytochrome family of plant photoreceptors, phyA and phyB, are epistatic to tfl2 in far-red and red light, respectively. An overlap between genes regulated by light and by auxin has earlier been reported and, in tfl2 plants light-dependent auxin-regulated genes are misexpressed. Further, we show that TFL2 binds to IAA5 and IAA19 suggesting that TFL2 might be involved in regulation of phytochrome-mediated light responses through auxin action.

  • 44.
    Valdés, Ana Elisa
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany.
    Roberts, Christina
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany.
    Carlsbecker, Annelie
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany.
    HD-Zip class III transcription factors control root development through the modulation of ROS levels2013Conference paper (Refereed)
  • 45.
    Valdés, Ana Elisa
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany.
    Roberts, Christina
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany.
    Carlsbecker, Annelie
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany.
    HD-Zip class III transcription factors control root development through the modulation of ROS levels2013Conference paper (Other academic)
    Abstract [en]

    In the Arabidopsis root the distinct spatial distribution of two ROS species, hydrogen peroxide and superoxide, controls a dynamic balance between cell division and cell differentiation. Superoxide accumulates in the root meristem while hydrogen peroxide accumulates in the elongation and differentiation zone. The balance between both species controls cell proliferation. Mutants defective in the developmental control regulators encoded by Class III homeodomain leucine zipper (HD-ZIP III) genes display alterations both in root growth rates and levels of ROS species. A gain-of-function mutant of the PHB HD-Zip III gene presents a short root length and small meristem size, while the multiple loss of HD-Zip genes functionality results in bigger root meristem size. Additionally, gain- and loss-of function mutants present contrasting ROS balances. Our analyses of transcriptome changes upon depleting HD-Zip III levels suggest that the HD-Zip class III transcription factors act upstream of ROS-related genetic pathways controlling meristem size and growth rate. Thus, the HD-Zip transcription factors may act to control root growth, possibly by modulation of ROS levels.

  • 46.
    Valdés, Ana Elisa
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany.
    Övernäs, Elin
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany.
    Johansson, Henrik
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany.
    Rada-Iglesias, Alvaro
    Engström, Peter
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany.
    The homeodomain-leucine zipper (HD-Zip) class I transcription factors ATHB7 and ATHB12 modulate abscisic acid signalling by regulating protein phosphatase 2C and abscisic acid receptor gene activities2012In: Plant Molecular Biology, ISSN 0167-4412, E-ISSN 1573-5028, Vol. 80, no 4-5, p. 405-418Article in journal (Refereed)
    Abstract [en]

    Plants perceiving drought activate multiple responses to improve survival, including large-scale alterations in gene expression. This article reports on the roles in the drought response of two Arabidopsis thaliana homeodomain-leucine zipper class I genes; ATHB7 and ATHB12, both strongly induced by water-deficit and abscisic acid (ABA). ABA-mediated transcriptional regulation of both genes is shown to depend on the activity of protein phosphatases type 2C (PP2C). ATHB7 and ATHB12 are, thus, targets of the ABA signalling mechanism defined by the PP2Cs and the PYR/PYL family of ABA receptors, with which the PP2C proteins interact. Our results from chromatin immunoprecipitation and gene expression analyses demonstrate that ATHB7 and ATHB12 act as positive transcriptional regulators of PP2C genes, and thereby as negative regulators of abscisic acid signalling. In support of this notion, our results also show that ATHB7 and ATHB12 act to repress the transcription of genes encoding the ABA receptors PYL5 and PYL8 in response to an ABA stimulus. In summary, we demonstrate that ATHB7 and ATHB12 have essential functions in the primary response to drought, as mediators of a negative feedback effect on ABA signalling in the plant response to water deficit.

  • 47. Vaten, Anne
    et al.
    Dettmer, Jan
    Wu, Shuang
    Stierhof, York-Dieter
    Miyashima, Shunsuke
    Yadav, Shri Ram
    Roberts, Christina J.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany.
    Campilho, Ana
    Bulone, Vincent
    Lichtenberger, Raffael
    Lehesranta, Satu
    Mahonen, Ari Pekka
    Kim, Jae-Yean
    Jokitalo, Eija
    Sauer, Norbert
    Scheres, Ben
    Nakajima, Keiji
    Carlsbecker, Annelie
    Gallagher, Kimberly L.
    Helariutta, Yka
    Callose Biosynthesis Regulates Symplastic Trafficking during Root Development2011In: Developmental Cell, ISSN 1534-5807, E-ISSN 1878-1551, Vol. 21, no 6, p. 1144-1155Article in journal (Refereed)
    Abstract [en]

    Plant cells are connected through plasmodesmata (PD), membrane-lined channels that allow symplastic movement of molecules between cells. However, little is known about the role of PD-mediated signaling during plant morphogenesis. Here, we describe an Arabidopsis gene, CALS3/GSL12. Gain-of-function mutations in CALS3 result in increased accumulation of callose (beta-1,3-glucan) at the PD, a decrease in PD aperture, defects in root development, and reduced intercellular trafficking. Enhancement of CALS3 expression during phloem development suppressed loss-of-function mutations in the phloem abundant callose synthase, CALS7 indicating that CALS3 is a bona fide callose synthase. CALS3 alleles allowed us to spatially and temporally control the PD aperture between plant tissues. Using this tool, we are able to show that movement of the transcription factor SHORT-ROOT and microRNA1 65 between the stele and the endodermis is PD dependent. Taken together, we conclude that regulated callose biosynthesis at PD is essential for cell signaling.

  • 48.
    Zhou, Shun-Fan
    et al.
    Fudan Univ, Sch Life Sci, Inst Plant Biol, Collaborat Innovat Ctr Genet & Dev,State Key Lab, Shanghai 200433, Peoples R China..
    Sun, Le
    Fudan Univ, Sch Life Sci, Inst Plant Biol, Collaborat Innovat Ctr Genet & Dev,State Key Lab, Shanghai 200433, Peoples R China..
    Valdes, Ana Elisa
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany.
    Engström, Peter
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany.
    Song, Ze-Ting
    Fudan Univ, Sch Life Sci, Inst Plant Biol, Collaborat Innovat Ctr Genet & Dev,State Key Lab, Shanghai 200433, Peoples R China..
    Lu, Sun-Jie
    Fudan Univ, Sch Life Sci, Inst Plant Biol, Collaborat Innovat Ctr Genet & Dev,State Key Lab, Shanghai 200433, Peoples R China..
    Liu, Jian-Xiang
    Fudan Univ, Sch Life Sci, Inst Plant Biol, Collaborat Innovat Ctr Genet & Dev,State Key Lab, Shanghai 200433, Peoples R China..
    Membrane-associated transcription factor peptidase, site-2 protease, antagonizes ABA signaling in Arabidopsis2015In: New Phytologist, ISSN 0028-646X, E-ISSN 1469-8137, Vol. 208, no 1, p. 188-197Article in journal (Refereed)
    Abstract [en]

    Abscisic acid plays important roles in maintaining seed dormancy while gibberellins (GA) and other phytohormones antagonize ABA to promote germination. However, how ABA signaling is desensitized during the transition from dormancy to germination is still poorly understood. We functionally characterized the role of membrane-associated transcription factor peptidase, site-2 protease (S2P), in ABA signaling during seed germination in Arabidopsis. Genetic analysis showed that loss-of-function of S2P conferred high ABA sensitivity during seed germination, and expression of the activated form of membrane-associated transcription factor bZIP17, in which the transmembrane domain and endoplasmic reticulum (ER) lumen-facing C-terminus were deleted, in the S2P mutant rescued its ABA-sensitive phenotype. MYC and green fluorescent protein (GFP)-tagged bZIP17 were processed and translocated from the ER to the nucleus in response to ABA treatment. Furthermore, genes encoding negative regulators of ABA signaling, such as the transcription factor ATHB7 and its target genes HAB1, HAB2, HAI1 and AHG3, were up-regulated in seeds of the wild-type upon ABA treatment; this up-regulation was impaired in seeds of S2P mutants. Our results suggest that S2P desensitizes ABA signaling during seed germination through regulating the activation of the membrane-associated transcription factor bZIP17 and therefore controlling the expression level of genes encoding negative regulators of ABA signaling.

  • 49. Álvarez-Buylla, Elena R.
    et al.
    Ambrose, Barbara A.
    Flores-Sandoval, Eduardo
    Vergara-Silva, Francisco
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organism Biology, Physiological Botany.
    Englund, Marie
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organism Biology, Physiological Botany.
    Garay-Arroyo, Adriana
    García-Ponce, Berenice
    de la Torre-Bárcena, Eduardo
    Espinosa-Matías, Silvia
    Martínez, Esteban
    Piñeyro-Nelson, Alma
    Engström, Peter
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organism Biology, Physiological Botany.
    Meyerowitz, Elliot M.
    B-Function Expression in the Flower Center Underlies the Homeotic Phenotype of Lacandonia schismatica (Triuridaceae)2010In: The Plant Cell, ISSN 1040-4651, E-ISSN 1532-298X, Vol. 22, no 11, p. 3543-3559Article in journal (Refereed)
    Abstract [en]

    Spontaneous homeotic transformations have been described in natural populations of both plants and animals, but little is known about the molecular-genetic mechanisms underlying these processes in plants. In the ABC model of floral organ identity in Arabidopsis thaliana, the B- and C-functions are necessary for stamen morphogenesis, and C alone is required for carpel identity. We provide ABC model-based molecular-genetic evidence that explains the unique inside-out homeotic floral organ arrangement of the monocotyledonous mycoheterotroph species Lacandonia schismatica (Triuridaceae) from Mexico. Whereas a quarter million flowering plant species bear central carpels surrounded by stamens, L. schismatica stamens occur in the center of the flower and are surrounded by carpels. The simplest explanation for this is that the B-function is displaced toward the flower center. Our analyses of the spatio-temporal pattern of B- and C-function gene expression are consistent with this hypothesis. The hypothesis is further supported by conservation between the B-function genes of L. schismatica and Arabidopsis, as the former are able to rescue stamens in Arabidopsis transgenic complementation lines, and Ls-AP3 and Ls-PI are able to interact with each other and with the corresponding Arabidopsis B-function proteins in yeast. Thus, relatively simple molecular modifications may underlie important morphological shifts in natural populations of extant plant taxa.

  • 50.
    Övernäs, Elin
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organism Biology, Physiological Botany.
    Characterisation of Members of the HD-Zip I and DREB/ERF Transcription Factor Families and their Functions in Plant Stress Responses2010Doctoral thesis, comprehensive summary (Other academic)
    Abstract [en]

    Plants have to adapt to various environmental conditions. In comparison with other eukaryotes, plant genomes encode relatively many transcription factors, and have families of transcription factors only found in plants, two such are the large AP2/ERF (APETALA2/Ethylene Responsive Factor) and HD-Zip (Homeodomain leucine zipper) families. Members of these families play roles in plant development, responses to stress and other environmental stimuli. This thesis describes the functions of members of both these families. Two AP2/ERF proteins of the DREB/ERF (Drought Responsive Element Binding/Ethylene Responsive Factor) subfamily, AtERF38 and AtERF39 show a negative effect on growth in transgenic over-expression lines. They are regulated by stress and confer stress tolerance, which suggests a function as negative growth regulators during stress. The 14 Oryza sativa (rice) HD-Zip I genes were described and a phylogenetic analysis of the HD-Zip I genes in Arabidopsis thaliana, rice and Craterostigma plantagineum defined four clades that were conserved between mono and dicots, but also showed that four clades had most likely been lost in either lineage. The phylogeny was supported by conserved intron/exon patterning and the duplication history of the rice genome. The expression patterns in different organs indicate a non-conserved regulation of genes within and between clades. Drought stress regulation was conserved within two clades, but not between the clades. Further analysis on the function of four HD-Zip I genes in Arabidopsis, ATHB5, -6, -7 and -12 showed an involvement in the transcriptional regulation of ABA receptors and signalling components. These are the first described direct target genes for ATHB7 and ATHB12. It was also shown that there exists a direct cross-regulation between these four HD-Zips. The effect of ATHB5, -6, -7 and -12 would be as negative regulators of ABA signalling, desensitising the plant to constant levels of ABA, and enabling sensitivity to changes in stress level.

    List of papers
    1. Two AP2 transcription factors, AtERF38 and AtERF39, have similar function but are differently regulated in ABA and stress responses.
    Open this publication in new window or tab >>Two AP2 transcription factors, AtERF38 and AtERF39, have similar function but are differently regulated in ABA and stress responses.
    (English)Manuscript (preprint) (Other academic)
    Research subject
    Physiological Botany
    Identifiers
    urn:nbn:se:uu:diva-129183 (URN)
    Available from: 2010-08-09 Created: 2010-08-06 Last updated: 2010-08-09
    2. A genome-wide survey of HD-Zip genes in rice and analysis of drought-responsive family members
    Open this publication in new window or tab >>A genome-wide survey of HD-Zip genes in rice and analysis of drought-responsive family members
    Show others...
    2008 (English)In: Plant Molecular Biology, ISSN 0167-4412, E-ISSN 1573-5028, Vol. 66, no 1-2, p. 87-103Article in journal (Refereed) Published
    Abstract [en]

    The homeodomain leucine zipper (HD-Zip) genes encode transcription factors that have diverse functions in plant development and have often been implicated in stress adaptation. The HD-Zip genes are the most abundant group of homeobox (HB) genes in plants and do not occur in other eukaryotes. This paper describes the complete annotation of the HD-Zip families I, II and III from rice and compares these gene families with Arabidopsis in a phylogeny reconstruction. Orthologous pairs of rice and Arabidopsis HD-Zip genes were predicted based on neighbour joining and maximum parsimony (MP) trees with support of conserved intron-exon organization. Additionally, a number of HD-Zip genes appeared to be unique to rice. Searching of EST and cDNA databases and expression analysis using RT-PCR showed that 30 out of 31 predicted rice HD-Zip genes are expressed. Most HD-Zip genes were broadly expressed in mature plants and seedlings, but others showed more organ specific patterns. Like in Arabidopsis and other dicots, a subset of the rice HD-Zip I and II genes was found to be regulated by drought stress. We identified both drought-induced and drought-repressed HD-Zip genes and demonstrate that these genes are differentially regulated in drought-sensitive versus drought-tolerant rice cultivars. The drought-repressed HD-Zip family I gene, Oshox4, was selected for promoter-GUS analysis, showing that drought-responsiveness of Oshox4 is controlled by the promoter and that Oshox4 expression is predominantly vascular-specific. Loss-of-function analysis of Oshox4 revealed no specific phenotype, but overexpression analysis suggested a role for Oshox4 in elongation and maturation processes.

    Keywords
    homeodomain-leucine zipper, homeobox, rice, Arabidopsis, drought
    National Category
    Biological Sciences
    Identifiers
    urn:nbn:se:uu:diva-13056 (URN)10.1007/s11103-007-9255-7 (DOI)000251656400007 ()17999151 (PubMedID)
    Available from: 2008-05-28 Created: 2008-05-28 Last updated: 2017-12-11Bibliographically approved
    3. The homeodomain-leucine zipper (HD-Zip) class I transcription factors ATHB7 and ATHB12 modulate abscisic acid signalling by regulating protein phosphatase 2C and abscisic acid receptor gene activities
    Open this publication in new window or tab >>The homeodomain-leucine zipper (HD-Zip) class I transcription factors ATHB7 and ATHB12 modulate abscisic acid signalling by regulating protein phosphatase 2C and abscisic acid receptor gene activities
    Show others...
    2012 (English)In: Plant Molecular Biology, ISSN 0167-4412, E-ISSN 1573-5028, Vol. 80, no 4-5, p. 405-418Article in journal (Refereed) Published
    Abstract [en]

    Plants perceiving drought activate multiple responses to improve survival, including large-scale alterations in gene expression. This article reports on the roles in the drought response of two Arabidopsis thaliana homeodomain-leucine zipper class I genes; ATHB7 and ATHB12, both strongly induced by water-deficit and abscisic acid (ABA). ABA-mediated transcriptional regulation of both genes is shown to depend on the activity of protein phosphatases type 2C (PP2C). ATHB7 and ATHB12 are, thus, targets of the ABA signalling mechanism defined by the PP2Cs and the PYR/PYL family of ABA receptors, with which the PP2C proteins interact. Our results from chromatin immunoprecipitation and gene expression analyses demonstrate that ATHB7 and ATHB12 act as positive transcriptional regulators of PP2C genes, and thereby as negative regulators of abscisic acid signalling. In support of this notion, our results also show that ATHB7 and ATHB12 act to repress the transcription of genes encoding the ABA receptors PYL5 and PYL8 in response to an ABA stimulus. In summary, we demonstrate that ATHB7 and ATHB12 have essential functions in the primary response to drought, as mediators of a negative feedback effect on ABA signalling in the plant response to water deficit.

    Keywords
    ABA, ABA receptors, Drought stress response, HD-Zip, PP2C, SnRK2
    National Category
    Natural Sciences
    Identifiers
    urn:nbn:se:uu:diva-129184 (URN)10.1007/s11103-012-9956-4 (DOI)000312133800004 ()
    Available from: 2010-08-09 Created: 2010-08-06 Last updated: 2017-12-12Bibliographically approved
    4. Involvement of the Arabidopsis HD-Zip genes ATHB5 and ATHB6 in ABA responses
    Open this publication in new window or tab >>Involvement of the Arabidopsis HD-Zip genes ATHB5 and ATHB6 in ABA responses
    (English)Manuscript (preprint) (Other academic)
    Identifiers
    urn:nbn:se:uu:diva-129185 (URN)
    Available from: 2010-08-09 Created: 2010-08-06 Last updated: 2016-04-25
12 1 - 50 of 52
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