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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.

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  • 2.
    Augstein, Frauke
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany.
    Mechanisms of plant root xylem developmental plasticity in response to water deficiency and salt2022Doctoral thesis, comprehensive summary (Other academic)
    Abstract [en]

    Plants may be exposed to a variety of different environmental conditions including water deficiency and salt, both affecting the uptake of water into the plant. Water is taken up from the soil by the roots and distributed throughout the plant via the water conducting tissue, the xylem. Plants are remarkably plastic and have evolved different mechanisms to sense the environment and adjust their development accordingly. However, how xylem development may respond to water availability is not clear. In this thesis, I show how water deficiency and salt affect xylem development and how the observed phenotypic alterations are regulated on a molecular level. We found that upon water deficiency additional protoxylem strands were formed along with an early differentiation of the inner metaxylem. These phenotypes were regulated both by non-cell autonomous and cell autonomous signaling via the hormone abscisic acid (ABA). The expression of microRNA165 was induced by ABA signaling in the endodermis leading to downregulation of homeo domain leucine zipper class III (HD-ZIP III) transcription factors in the stele. This caused a shift in xylem identity from meta- to protoxylem and the formation of additional protoxylem strands. At the same time, cell autonomous ABA signaling upregulated several VASCULAR RELATED NAC DOMAIN (VND) transcription factors including VND7, which promoted the shift in xylem identity as well as VND2 and VND3, which promoted early differentiation of the inner metaxylem. In contrast, during an initial phase of salt stress, we observed the formation of protoxylem gaps specifically in response to ionic stress and distinct from ABA-signaling. We identified that protoxylem gaps were caused by lowered levels and signaling of the growth regulator gibberellin (GA). Downstream of GA-signaling, protoxylem gap formation upon salt was controlled by genes involved in secondary cell wall formation including the xylem master regulator VND6 and factors involved in cell wall modification. Salt tolerance assays suggested that protoxylem gaps may contribute to salt tolerance and the phenotypes that we observed upon water deficiency have been suggested to confer drought tolerance. We observed similar effects on xylem developmental plasticity in response to water deficiency and salt in various different dicot species indicating an evolutionary conservation. Thus, xylem development is of high relevance for breeding programs to generate plant varieties better adapted to a changing climate.

    List of papers
    1. Continuous root xylem formation and vascular acclimation to water deficit involves endodermal ABA signalling via miR165
    Open this publication in new window or tab >>Continuous root xylem formation and vascular acclimation to water deficit involves endodermal ABA signalling via miR165
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    2018 (English)In: Development, ISSN 0950-1991, E-ISSN 1477-9129, Vol. 145, no 3, article id dev159202Article in journal (Refereed) Published
    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.

    Place, publisher, year, edition, pages
    COMPANY OF BIOLOGISTS LTD, 2018
    Keywords
    ABA, Arabidopsis thaliana, HD-ZIP III transcription factors, miR165, Xylem
    National Category
    Biological Sciences
    Identifiers
    urn:nbn:se:uu:diva-347084 (URN)10.1242/dev.159202 (DOI)000424653300014 ()
    Available from: 2018-03-27 Created: 2018-03-27 Last updated: 2022-01-28Bibliographically approved
    2. Abscisic acid signaling activates distinct VND transcription factors to promote xylem differentiation in Arabidopsis
    Open this publication in new window or tab >>Abscisic acid signaling activates distinct VND transcription factors to promote xylem differentiation in Arabidopsis
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    2021 (English)In: Current Biology, ISSN 0960-9822, E-ISSN 1879-0445, Vol. 31, no 14, p. 3153-3161.e5Article in journal (Refereed) Published
    Abstract [en]

    Plants display remarkable abilities to adjust growth and development to environmental conditions, such as the amount of available water. This developmental plasticity is apparent not only in root and shoot growth rates, but also in tissue patterning and cell morphology.(1,2) We have previously shown that in response to limited water availability, Arabidopsis thaliana root displays changes in xylem morphology, mediated by the non-cell-autonomous action of abscisic acid, ABA.(2) Here, we show, through analyses of ABA response reporters and tissue-specific suppression of ABA signaling, that xylem cells themselves act as primary signaling centers governing both xylemcell fate and xylem differentiation rate, revealing the cell-autonomous control of multiple aspects of xylem development by ABA. ABA rapidly activates the expression of genes encoding VASCULAR-RELATED NAC DOMAIN (VND) transcription factors. Molecular and genetic analyses revealed that the two ABA-mediated xylem developmental changes are regulated by distinct members of this transcription factor family, with VND2 and VND3 promoting differentiation rate of metaxylem cells, while VND7 promotes the conversion of metaxylem toward protoxylem morphology. This phenomenon shows how different aspects of developmental plasticity can be interlinked, yet genetically separable. Moreover, similarities in phenotypic and molecular responses to ABA in diverse species indicate evolutionary conservation of the ABA-xylem development regulatory network among eudicots. Hence, this study gives molecular insights into how environmental stress modifies plant vascular anatomy and has potential relevance for water use optimization and adaptation to drought conditions.

    Place, publisher, year, edition, pages
    Cell PressCELL PRESS, 2021
    National Category
    Botany
    Identifiers
    urn:nbn:se:uu:diva-452373 (URN)10.1016/j.cub.2021.04.057 (DOI)000678562700015 ()34043949 (PubMedID)
    Funder
    Swedish Research Council, 201705122Swedish Research Council Formas, 201700857Stiftelsen Akademiens Nilsson-Ehle medaljKnut and Alice Wallenberg Foundation, KAW2016.0274
    Available from: 2021-09-07 Created: 2021-09-07 Last updated: 2024-01-15Bibliographically approved
    3. DELLA-regulated root xylem developmental response to salt stress in Arabidopsis
    Open this publication in new window or tab >>DELLA-regulated root xylem developmental response to salt stress in Arabidopsis
    (English)Manuscript (preprint) (Other academic)
    Abstract [en]

    Salinity impairs plant growth and leads to reduction in yield in many crop species. Salt reduces water availability and exposes the plant to ion toxicity. However, plants exhibit an incredible developmental plasticity to adjust to environmental stresses, and xylem development can respond to water limitation with enhanced xylem differentiation rates and alterations in xylem cell morphology. Here, we report that salinity triggers a distinct response, with the formation of discontinuous protoxylem, protoxylem gaps, in Arabidopsis seedlings. The formation of protoxylem gaps may confer enhanced tolerance to salt, as mutants exhibiting more protoxylem gaps survive salt stress better, while mutants not forming xylem gaps are less tolerant. We present results suggesting that salt induces protoxylem gaps as a consequence of reduced gibberellin levels and signaling, and protoxylem gap formation is suppressed in the della quintuple mutant, in which GA signaling is no longer under DELLA repression. Transcriptome analysis upon salt stress in the della quintuple mutant revealed a previously unknown role for the xylem master regulator VASCULAR RELATED NAC DOMAIN 6 (VND6) in protoxylem gap formation. With VND6 several factors involved in secondary cell wall formation or cell wall modification were differentially expressed upon salt, including several alfa expansins. Seedlings of both salt sensitive and salt tolerant eudicot species form protoxylem gaps upon salt stress, suggesting that this response is conserved among eudicot species.

    Keywords
    Arabidopsis, DELLA, gibberellin, root, salt, xylem
    National Category
    Botany Developmental Biology Biochemistry and Molecular Biology
    Research subject
    Biology with specialization in Physiological Botany
    Identifiers
    urn:nbn:se:uu:diva-466393 (URN)
    Funder
    Swedish Research Council Formas, 2017-00857
    Available from: 2022-01-27 Created: 2022-01-27 Last updated: 2022-02-22Bibliographically approved
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  • 3.
    Augstein, Frauke
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany. Linnean Centre for Plant Biology, Uppsala, Sweden.
    Carlsbecker, Annelie
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany. Linnean Centre for Plant Biology, Uppsala, Sweden.
    DELLA-regulated root xylem developmental response to salt stress in ArabidopsisManuscript (preprint) (Other academic)
    Abstract [en]

    Salinity impairs plant growth and leads to reduction in yield in many crop species. Salt reduces water availability and exposes the plant to ion toxicity. However, plants exhibit an incredible developmental plasticity to adjust to environmental stresses, and xylem development can respond to water limitation with enhanced xylem differentiation rates and alterations in xylem cell morphology. Here, we report that salinity triggers a distinct response, with the formation of discontinuous protoxylem, protoxylem gaps, in Arabidopsis seedlings. The formation of protoxylem gaps may confer enhanced tolerance to salt, as mutants exhibiting more protoxylem gaps survive salt stress better, while mutants not forming xylem gaps are less tolerant. We present results suggesting that salt induces protoxylem gaps as a consequence of reduced gibberellin levels and signaling, and protoxylem gap formation is suppressed in the della quintuple mutant, in which GA signaling is no longer under DELLA repression. Transcriptome analysis upon salt stress in the della quintuple mutant revealed a previously unknown role for the xylem master regulator VASCULAR RELATED NAC DOMAIN 6 (VND6) in protoxylem gap formation. With VND6 several factors involved in secondary cell wall formation or cell wall modification were differentially expressed upon salt, including several alfa expansins. Seedlings of both salt sensitive and salt tolerant eudicot species form protoxylem gaps upon salt stress, suggesting that this response is conserved among eudicot species.

  • 4.
    Augstein, Frauke
    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.
    Getting to the Roots: A Developmental Genetic View of Root Anatomy and Function From Arabidopsis to Lycophytes2018In: Frontiers in Plant Science, E-ISSN 1664-462X, Vol. 9, article id 1410Article, review/survey (Refereed)
    Abstract [en]

    Roots attach plants to the ground and ensure efficient and selective uptake of water and nutrients. These functions are facilitated by the morphological and anatomical structures of the root, formed by the activity of the root apical meristem (RAM) and consecutive patterning and differentiation of specific tissues with distinct functions. Despite the importance of this plant organ, its evolutionary history is not clear, but fossils suggest that roots evolved at least twice, in the lycophyte (clubmosses and their allies) and in the euphyllophyte (ferns and seed plants) lineages. Both lycophyte and euphyllophyte roots grow indeterminately by the action of an apical meristem, which is protected by a root cap. They produce root hairs, and in most species the vascular stele is guarded by a specialized endodermal cell layer. Hence, most of these traits must have evolved independently in these lineages. This raises the question if the development of these apparently analogous tissues is regulated by distinct or homologous genes, independently recruited from a common ancestor of lycophytes and euphyllophytes. Currently, there are few studies of the genetic and molecular regulation of lycophyte and fern roots. Therefore, in this review, we focus on key regulatory networks that operate in root development in the model angiosperm Arabidopsis. We describe current knowledge of the mechanisms governing RAM maintenance as well as patterning and differentiation of tissues, such as the endodermis and the vasculature, and compare with other species. We discuss the importance of comparative analyses of anatomy and morphology of extant and extinct species, along with analyses of gene regulatory networks and, ultimately, gene function in plants holding key phylogenetic positions to test hypotheses of root evolution.

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  • 5.
    Augstein, Frauke
    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.
    Salinity induces discontinuous protoxylem via a DELLA-dependent mechanism promoting salt tolerance in Arabidopsis seedlings2022In: New Phytologist, ISSN 0028-646X, E-ISSN 1469-8137, Vol. 236, no 1, p. 195-209Article in journal (Refereed)
    Abstract [en]
    • Salinity is detrimental to plants and developmental adjustments limiting salt uptake and transport is therefore important for acclimation to high salt. These parameters may be influenced by xylem morphology, however how plant root xylem development is affected by salt stress remains unclear.

    • Using molecular and genetic techniques and detailed phenotypic analyses, we demonstrate that salt causes distinct effects on Arabidopsis seedling root xylem and reveal underlying molecular mechanisms.

    • Salinity causes intermittent inhibition of protoxylem cell differentiation, generating protoxylem gaps, in Arabidopsis and several other eudicot seedlings. The extent of protoxylem gaps in seedlings positively correlates with salt tolerance. Reduced gibberellin signalling is required for protoxylem gap formation. Mutant analyses reveal that the xylem differentiation regulator VASCULAR RELATED NAC DOMAIN 6 (VND6), along with secondary cell wall producing and cell wall modifying enzymes, including EXPANSIN A1 (EXP1), are involved in protoxylem gap formation, in a DELLA-dependent manner.

    • Salt stress is likely to reduce levels of bioactive gibberellins, stabilising DELLAs, which in turn activates multiple factors modifying protoxylem differentiation. Salt stress impacts seedling survival and formation of protoxylem gaps may be a measure to enhance salt tolerance.

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  • 6.
    Barcelo, Marta
    et al.
    IFAPA Ctr Malaga, Cortijo Cruz S-N, Malaga 29140, Spain.
    Wallin, Anita
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany.
    Medina, Juan J.
    IFAPA Ctr Torres Tomejfl, Seville 41200, Spain.
    Gil-Ariza, David J.
    IFAPA Ctr Malaga, Cortijo Cruz S-N, Malaga 29140, Spain.
    Lopez-Casado, Gloria
    Univ Malaga, Dept Biol Vegetal, Inst Hortofruticultura Subtrop & Mediterranea La, E-29071 Malaga, Spain.
    Juarez, Jose
    Ctra Moncada Naquera, IVIA, Km 4-5, Valencia 46113, Spain.
    Sanchez-Sevilla, Jose F.
    IFAPA Ctr Malaga, Cortijo Cruz S-N, Malaga 29140, Spain.
    Lopez-Encina, Carlos
    Inst Hortofruticultura Subtrop & Mediterranea La, Malaga 29750, Spain.
    Lopez-Aranda, Jose M.
    IFAPA Ctr Malaga, Cortijo Cruz S-N, Malaga 29140, Spain.
    Mercado, Jose A.
    Univ Malaga, Dept Biol Vegetal, Inst Hortofruticultura Subtrop & Mediterranea La, E-29071 Malaga, Spain.
    Pliego-Alfaro, Fernando
    Univ Malaga, Dept Biol Vegetal, Inst Hortofruticultura Subtrop & Mediterranea La, E-29071 Malaga, Spain.
    Isolation and culture of strawberry protoplasts and field evaluation of regenerated plants2019In: Scientia Horticulturae, ISSN 0304-4238, E-ISSN 1879-1018, Vol. 256, article id 108552Article in journal (Refereed)
    Abstract [en]

    Protoplasts are an useful biotechnological tool for plant improvement In strawberry, very few studies on protoplast technology have been carried out. In this investigation, a procedure for the isolation and culture of strawberry protoplasts, cv. 'Chandler', has been developed. The effect of several factors affecting the successful isolation of protoplasts and formation of microcalli, e.g. explant source, washing procedure, hormonal composition of the culture medium and protoplast density, were evaluated. For shoot regeneration, microcalli derived from isolated protoplasts were transferred to MS medium supplemented with 0.2 mg l(-1) NAA and either 5 mg l(-1) BA or 3 mgl(-1) TDZ, obtaining a similar regeneration rate, 17%, in both media. Twenty-one independent protoclones were transferred to field conditions for agronomic evaluation. Significant alterations in the growth habit, density of foliage, leaf color and leaf morphology were detected in some lines. Fruit yield was significantly reduced in 15 out of the 21 protoclones evaluated due to a reduction in fruit weight and/or the number of fruits. Ploidy level was unaffected in a sample of 6 lines selected at random; however, a study of genetic stability by using 10 EST-SSR markers showed genetic alterations in all the lines analyzed. Despite the high rate of somaclonal variation detected in the protoclones, some of the lines displayed an agronomical behavior similar to control plants, indicating that this protocol could be useful for genetic improvement in this species.

  • 7.
    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, 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.

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  • 8.
    Carlsbecker, Annelie
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany.
    Augstein, Frauke
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany.
    Xylem versus phloem in secondary growth: a balancing act mediated by gibberellins2021In: Journal of Experimental Botany, ISSN 0022-0957, E-ISSN 1460-2431, Vol. 72, no 10, p. 3489-3492Article in journal (Other academic)
    Abstract [en]

    Secondary growth generates wood, which constitutes most of the plant biomass. Despite considerable efforts over the last decade to uncover the genetic and molecular regulation of the vascular cambium, there is still much to learn about how it produces wood (xylem) inward and bast (phloem) outward. Ben-Targem et al. (2021) now provide novel insight into how the hormones auxin and gibberellic acid (GA) govern the activity of the cambium, promoting a transition from formation of equal amounts of xylem and phloem to a stage where xylem formation dominates phloem in Arabidopsis hypocotyls, resembling wood formation in trees.

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  • 9.
    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.

  • 10.
    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)
  • 11.
    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.

  • 12. 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.

  • 13.
    Engelsdorf, Timo
    et al.
    Norwegian Univ Sci & Technol, Hogskoleringen 5, Dept Biol, N-7491 Trondheim, Norway;Philipps Univ Marburg, Dept Biol, Div Plant Physiol, D-35043 Marburg, Germany.
    Gigli-Bisceglia, Nora
    Norwegian Univ Sci & Technol, Hogskoleringen 5, Dept Biol, N-7491 Trondheim, Norway.
    Veerabagu, Manikandan
    Norwegian Univ Sci & Technol, Hogskoleringen 5, Dept Biol, N-7491 Trondheim, Norway;Norwegian Univ Life Sci, Dept Plant Sci, N-1432 As, Norway.
    McKenna, Joseph F.
    Imperial Coll London, Dept Biol, South Kensington Campus, London SW7 2AZ, England;Oxford Brookes Univ, Dept Biol & Med Sci, Plant Cell Biol, Oxford OX3 0BP, England.
    Vaahtera, Lauri
    Norwegian Univ Sci & Technol, Hogskoleringen 5, Dept Biol, N-7491 Trondheim, Norway.
    Augstein, Frauke
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany. Norwegian Univ Sci & Technol, Hogskoleringen 5, Dept Biol, N-7491 Trondheim, Norway;Uppsala Univ, Linnean Ctr Plant Biol, Ullsv 24E, SE-75651 Uppsala, Sweden.
    Van der Does, Dieuwertje
    Norwich Res Pk, Sainsbury Lab, Norwich Res Pk, Norwich NR4 7UH, Norfolk, England;2Blades Fdn BecA ILRI Hub, POB 30709, Nairobi 00100, Kenya.
    Zipfel, Cyril
    Norwich Res Pk, Sainsbury Lab, Norwich Res Pk, Norwich NR4 7UH, Norfolk, England.
    Hamann, Thorsten
    Norwegian Univ Sci & Technol, Hogskoleringen 5, Dept Biol, N-7491 Trondheim, Norway.
    The plant cell wall integrity maintenance and immune signaling systems cooperate to control stress responses in Arabidopsis thaliana2018In: Science Signaling, ISSN 1945-0877, E-ISSN 1937-9145, Vol. 11, no 536, article id eaao3070Article in journal (Refereed)
    Abstract [en]

    Cell walls surround all plant cells, and their composition and structure are modified in a tightly controlled, adaptive manner to meet sometimes opposing functional requirements during growth and development. The plant cell wall integrity (CWI) maintenance mechanism controls these functional modifications, as well as responses to cell wall damage (CWD). We investigated how the CWI system mediates responses to CWD in Arabidopsis thaliana. CWD induced by cell wall-degrading enzymes or an inhibitor of cellulose biosynthesis elicited similar, turgor-sensitive stress responses. Phenotypic clustering with 27 genotypes identified a core group of receptor-like kinases (RLKs) and ion channels required for the activation of CWD responses. A genetic analysis showed that the RLK FEI2 and the plasma membrane-localized mechanosensitive Ca2+ channel MCA1 functioned downstream of the RLK THE1 in CWD perception. In contrast, pattern-triggered immunity (PTI) signaling components, including the receptors for plant elicitor peptides (AtPeps) PEPR1 and PEPR2, repressed responses to CWD. CWD induced the expression of PROPEP1 and PROPEP3, which encode the precursors of AtPep1 and AtPep3, and the release of PROPEP3 into the growth medium. Application of AtPep1 and AtPep3 repressed CWD-induced phytohormone accumulation in a concentration-dependent manner. These results suggest that AtPep-mediated signaling suppresses CWD-induced defense responses controlled by the CWI mechanism. This suppression was alleviated when PTI signaling downstream of PEPR1 and PEPR2 was impaired. Defense responses controlled by the CWI maintenance mechanism might thus compensate to some extent for the loss of PTI signaling elements.

  • 14.
    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.

  • 15.
    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.

  • 16.
    Gokulendran Nair, Akshay
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany. Uppsala University, Disciplinary Domain of Science and Technology, Biology, Biology Education Centre.
    The Enthralling Case of Root Xylem Developmental Plasticity in Arabidopsis thaliana Accessions upon ABA stress2021Independent thesis Advanced level (degree of Master (Two Years)), 40 credits / 60 HE creditsStudent thesis
    Abstract [en]

    The climate-changing scenario is affecting the global rainfall pattern, leading to drought and threatening crop production. The developmental plasticity in root vascular tissue in response to abiotic stress is largely unexplored. The stress hormone abscisic acid (ABA) promotes inner metaxylem and outer metaxylem differentiation closer to the root tip and also modulates outer metaxylem cell morphology. These xylem plasticity traits may play a crucial role in minimizing embolism in vascular tissues and improving root water uptake in plants. However, most of these xylem plasticity traits in response to abiotic stress are studied on the common laboratory-grown Arabidopsis accession Col-0. We evaluated phenotypic plasticity traits in root xylem tissue after ABA treatment in Arabidopsis accessions collected from wide geographical locations. Arabidopsis accessions demonstrated considerable variation in the initial site of imx differentiation and outer metaxylem cell fate change upon ABA treatment. Also, few Arabidopsis accessions displayed a well-differentiated outer metaxylem closer to the root tip under control conditions. The Arabidopsis accessions displaying enhanced imx differentiation differs from the accessions displaying extensive reticulate xylem trait upon ABA treatment. Suggesting, these two traits may not be linked. In addition, accessions showing inner metaxylem formation closer to the root tip are more sensitive to salinity stress. This study signifies the natural variations in Arabidopsis as a tool for highlighting distinct root xylem plasticity traits upon ABA stress.

    The full text will be freely available from 2025-11-07 13:34
  • 17.
    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, 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.

  • 18.
    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)
  • 19.
    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: 2022-01-28Bibliographically 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
    Download full text (pdf)
    FULLTEXT01
  • 20.
    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)
  • 21.
    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)
  • 22.
    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)
  • 23.
    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)
  • 24.
    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.

  • 25. 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.

  • 26.
    Lagercrantz, Ulf
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Plant Ecology and Evolution.
    Billhardt, Anja
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Plant Ecology and Evolution.
    Rousku, Sabine N.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Plant Ecology and Evolution.
    Landberg, Katarina
    Thelander, Mattias
    Eklund, D. Magnus
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Plant Ecology and Evolution. Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany.
    PIF-independent regulation of growth by an evening complex in the liverwort Marchantia polymorpha2022In: PLOS ONE, E-ISSN 1932-6203, Vol. 17, no 6, article id e0269984Article in journal (Refereed)
    Abstract [en]

    Previous studies in the liverwort Marchantia polymorpha have shown that the putative evening complex (EC) genes LUX ARRHYTHMO (LUX) and ELF4-LIKE (EFL) have a function in the liverwort circadian clock. Here, we studied the growth phenotypes of MpLUX and MpEFL loss-of-function mutants, to establish if PHYTOCHROME-INTERACTING FACTOR (PIF) and auxin act downstream of the M. polymorpha EC in a growth-related pathway similar to the one described for the flowering plant Arabidopsis. We examined growth rates and cell properties of loss-of-function mutants, analyzed protein-protein interactions and performed gene expression studies using reporter genes. Obtained data indicate that an EC can form in M. polymorpha and that this EC regulates growth of the thallus. Altered auxin levels in Mplux mutants could explain some of the phenotypes related to an increased thallus surface area. However, because MpPIF is not regulated by the EC, and because Mppif mutants do not show reduced growth, the growth phenotype of EC-mutants is likely not mediated via MpPIF. In Arabidopsis, the circadian clock regulates elongation growth via PIF and auxin, but this is likely not an evolutionarily conserved growth mechanism in land plants. Previous inventories of orthologs to Arabidopsis clock genes in various plant lineages showed that there is high levels of structural differences between clocks of different plant lineages. Here, we conclude that there is also variation in the output pathways used by the different plant clocks to control growth and development.

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  • 27.
    Lagercrantz, Ulf
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Plant Ecology and Evolution.
    Billhardt, Anja
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Plant Ecology and Evolution.
    Rousku, Sabine N.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Plant Ecology and Evolution.
    Leso, Martina
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Plant Ecology and Evolution.
    Reza, Salim Hossain
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Plant Ecology and Evolution.
    Eklund, D. Magnus
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Plant Ecology and Evolution. Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany.
    DE‐ETIOLATED1 has a role in the circadian clock of the liverwort Marchantia polymorpha2021In: New Phytologist, ISSN 0028-646X, E-ISSN 1469-8137, Vol. 232, no 2, p. 595-609Article in journal (Refereed)
    Abstract [en]

    Previous studies of plant circadian clock evolution have often relied on clock models and genes defined in Arabidopsis. These studies identified homologues with seemingly conserved function, as well as frequent gene loss. In the present study, we aimed to identify candidate clock genes in the liverwort Marchantia polymorpha using a more unbiased approach.

    To identify genes with circadian rhythm we sequenced the transcriptomes of gemmalings in a time series in constant light conditions. Subsequently, we performed functional studies using loss-of-function mutants and gene expression reporters.

    Among the genes displaying circadian rhythm, a homologue to the transcriptional co-repressor Arabidopsis DE-ETIOLATED1 showed high amplitude and morning phase. Because AtDET1 is arrhythmic and associated with the morning gene function of AtCCA1/LHY, that lack a homologue in liverworts, we functionally studied DET1 in M. polymorpha.

    We found that the circadian rhythm of MpDET1 expression is disrupted in loss-of-function mutants of core clock genes and putative evening-complex genes. MpDET1 knock-down in turn results in altered circadian rhythm of nyctinastic thallus movement and clock gene expression. We could not detect any effect of MpDET1 knock-down on circadian response to light, suggesting that MpDET1 has a yet unknown function in the M. polymorpha circadian clock.

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  • 28.
    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.

  • 29.
    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)
  • 30.
    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.))
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    Orizaola & Valdes SINC
  • 31.
    Ramachandran, Prashanth
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany. Linnean Centre for Plant Biology.
    Stelar Performance Under Drought: Regulation of Developmental Robustness and Plasticity of the Arabidopsis Root Xylem2020Doctoral thesis, comprehensive summary (Other academic)
    Abstract [en]

    Plants have evolved genetic mechanisms to sense, modulate and modify developmental programs in response to the changing environment. This brings forth challenges in stably generating tissue patterns while simultaneously allowing amenability. Gene perturbation studies have identified molecular regulators that control fate specification and differentiation of various tissues. However, we lack a complete understanding of how these processes are influenced by the environment. In this thesis, using Arabidopsis xylem as a model, I show that developmental regulators that function in maintaining a stable growth pattern are also involved in the manifestation of phenotypic plasticity. We found that the generation of a robust xylem developmental program is dependent on a feed forward loop between components of the auxin signalling pathway and the master regulators of xylem development, class III Homeodomain Leucine-Zipper (HD-ZIP III) transcription factors (TFs). By directly activating an auxin signalling activator (MP) and repressor (IAA20), the HD-ZIP III TFs facilitate stable xylem patterning and development. We also show that alterations to the HD-ZIP III mediated xylem developmental program were caused non-cell autonomously by changes in levels and signalling of a key regulator of abiotic stress response, abscisic acid (ABA). The suppression and enhancement of ABA signalling resulted in lower and higher levels respectively of mir165, a known post transcriptional regulator of HD-ZIP III levels. Under conditions of enhanced ABA signalling we found that ABA also acts cell autonomously through master regulators of xylem differentiation, VASCULAR RELATED NAC-DOMAIN (VND) transcription factors. Furthermore, we show that both cell autonomous and non-cell autonomous pathways are employed during water deficit conditions to alter xylem morphology and differentiation rate, likely to enhance water uptake. Taken together, our results show that ABA’s influence on evolutionarily conserved development regulators is important for xylem developmental plasticity. The identification of genetic regulators that control plant phenotypic alterations to limited water availability such as those identified in this thesis will be important to develop tolerant varieties that can survive the extended periods of drought caused by the alarming rise in global temperatures.

    List of papers
    1. PHABULOSA Mediates an Auxin Signaling Loop to Regulate Vascular Patterning in Arabidopsis
    Open this publication in new window or tab >>PHABULOSA Mediates an Auxin Signaling Loop to Regulate Vascular Patterning in Arabidopsis
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    2016 (English)In: Plant Physiology, ISSN 0032-0889, E-ISSN 1532-2548, Vol. 170, no 2, p. 956-970Article in journal (Refereed) Published
    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.

    National Category
    Botany
    Identifiers
    urn:nbn:se:uu:diva-279586 (URN)10.1104/pp.15.01204 (DOI)000369343300028 ()26637548 (PubMedID)
    Funder
    Swedish Research Council, 2010-5637Swedish Research Council Formas, 2007:1169Carl Tryggers foundation , CTS 07:64Carl Tryggers foundation , CTS 12:82Magnus Bergvall FoundationHelge Ax:son Johnsons stiftelse
    Available from: 2016-03-02 Created: 2016-03-02 Last updated: 2020-01-10Bibliographically approved
    2. Continuous root xylem formation and vascular acclimation to water deficit involves endodermal ABA signalling via miR165
    Open this publication in new window or tab >>Continuous root xylem formation and vascular acclimation to water deficit involves endodermal ABA signalling via miR165
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    2018 (English)In: Development, ISSN 0950-1991, E-ISSN 1477-9129, Vol. 145, no 3, article id dev159202Article in journal (Refereed) Published
    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.

    Place, publisher, year, edition, pages
    COMPANY OF BIOLOGISTS LTD, 2018
    Keywords
    ABA, Arabidopsis thaliana, HD-ZIP III transcription factors, miR165, Xylem
    National Category
    Biological Sciences
    Identifiers
    urn:nbn:se:uu:diva-347084 (URN)10.1242/dev.159202 (DOI)000424653300014 ()
    Available from: 2018-03-27 Created: 2018-03-27 Last updated: 2022-01-28Bibliographically approved
    3. Xylem developmental plasticity requires ABA mediated VND activation
    Open this publication in new window or tab >>Xylem developmental plasticity requires ABA mediated VND activation
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    (English)Manuscript (preprint) (Other academic)
    National Category
    Agricultural and Veterinary sciences Botany
    Identifiers
    urn:nbn:se:uu:diva-401799 (URN)
    Available from: 2020-01-09 Created: 2020-01-09 Last updated: 2020-04-23Bibliographically approved
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    presentationsbild
  • 32.
    Ramachandran, Prashanth
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany.
    Augstein, Frauke
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany.
    Mazumdar, Shamik
    Department of Plant Biology, Uppsala BioCenter, Linnean Center for Plant Biology, Swedish University of Agricultural Sciences.
    Nguyen, Van
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany.
    Minina, Elena A.
    Department of Molecular Sciences, Uppsala BioCenter, Linnean Center for Plant Biology, Swedish University of Agricultural Sciences..
    Melnyk, Charles
    Department of Plant Biology, Uppsala BioCenter, Linnean Center for Plant Biology, Swedish University of Agricultural Sciences.
    Carlsbecker, Annelie
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany.
    Xylem developmental plasticity requires ABA mediated VND activationManuscript (preprint) (Other academic)
  • 33.
    Ramachandran, Prashanth
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany. Stanford Univ, Dept Biol, 371 Jane Stanford Way, Stanford, CA 94305 USA..
    Augstein, Frauke
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany.
    Mazumdar, Shamik
    Swedish Univ Agr Sci, Dept Plant Biol, Linnean Ctr Plant Biol, Ullsv 24E, SE-75651 Uppsala, Sweden..
    Van Nguyen, Thanh
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany.
    Minina, Elena A.
    Swedish Univ Agr Sci, Dept Mol Sci, Linnean Ctr Plant Biol, Ullsv 24E, SE-75651 Uppsala, Sweden..
    Melnyk, Charles W.
    Swedish Univ Agr Sci, Dept Plant Biol, Linnean Ctr Plant Biol, Ullsv 24E, SE-75651 Uppsala, Sweden..
    Carlsbecker, Annelie
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany.
    Abscisic acid signaling activates distinct VND transcription factors to promote xylem differentiation in Arabidopsis2021