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Carlsbecker, Annelie
Publications (10 of 31) Show all publications
Ramachandran, P., Wang, G., Augstein, F., de Vries, J. & Carlsbecker, A. (2018). Continuous root xylem formation and vascular acclimation to water deficit involves endodermal ABA signalling via miR165. Development, 145(3), Article ID dev159202.
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: 2018-03-27Bibliographically approved
Augstein, F. & Carlsbecker, A. (2018). Getting to the Roots: A Developmental Genetic View of Root Anatomy and Function From Arabidopsis to Lycophytes. Frontiers in Plant Science, 9, Article ID 1410.
Open this publication in new window or tab >>Getting to the Roots: A Developmental Genetic View of Root Anatomy and Function From Arabidopsis to Lycophytes
2018 (English)In: Frontiers in Plant Science, ISSN 1664-462X, E-ISSN 1664-462X, Vol. 9, article id 1410Article, review/survey (Refereed) Published
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.

Keywords
roots, plant evo-devo, plant development, plant anatomy and morphology, patterning, gene regulatory network
National Category
Botany Developmental Biology
Identifiers
urn:nbn:se:uu:diva-366384 (URN)10.3389/fpls.2018.01410 (DOI)000445524300002 ()
Funder
Swedish Research Council Formas, 2013-953Swedish Research Council Formas, 2017-00857
Available from: 2018-11-22 Created: 2018-11-22 Last updated: 2018-11-22Bibliographically approved
Ramachandran, P., Carlsbecker, A. & Etchells, J. P. (2017). Class III HD- ZIPs govern vascular cell fate: an HD view on patterning and differentiation. Journal of Experimental Botany, 68(1), 55-69
Open this publication in new window or tab >>Class III HD- ZIPs govern vascular cell fate: an HD view on patterning and differentiation
2017 (English)In: Journal of Experimental Botany, ISSN 0022-0957, E-ISSN 1460-2431, Vol. 68, no 1, p. 55-69Article, review/survey (Refereed) Published
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.

Place, publisher, year, edition, pages
OXFORD UNIV PRESS, 2017
Keywords
Auxin, (pro)cambium, cytokinin, HD-ZIP III, miR165/166, root, shoot, transcription factors, vascular development, xylem
National Category
Botany
Identifiers
urn:nbn:se:uu:diva-321025 (URN)10.1093/jxb/erw370 (DOI)000397127100006 ()27794018 (PubMedID)
Funder
Swedish Research Council Formas, 2013-953EU, FP7, Seventh Framework Programme
Available from: 2017-04-28 Created: 2017-04-28 Last updated: 2017-04-28Bibliographically approved
de Vries, J., Fischer, A. M., Roettger, M., Rommel, S., Schluepmann, H., Bräutigam, A., . . . Gould, S. B. (2016). Cytokinin-induced promotion of root meristem size in the fern Azolla supports a shoot-like origin of euphyllophyte roots.. New Phytologist, 209(2), 705-720
Open this publication in new window or tab >>Cytokinin-induced promotion of root meristem size in the fern Azolla supports a shoot-like origin of euphyllophyte roots.
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2016 (English)In: New Phytologist, ISSN 0028-646X, E-ISSN 1469-8137, Vol. 209, no 2, p. 705-720Article in journal (Refereed) Published
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.

National Category
Natural Sciences
Identifiers
urn:nbn:se:uu:diva-287508 (URN)10.1111/nph.13630 (DOI)000373376500026 ()26358624 (PubMedID)
Available from: 2016-04-25 Created: 2016-04-25 Last updated: 2017-11-30Bibliographically approved
Müller, C. J., Valdés, A. E., Wang, G., Ramachandran, P., Beste, L., Uddenberg, D. & Carlsbecker, A. (2016). PHABULOSA Mediates an Auxin Signaling Loop to Regulate Vascular Patterning in Arabidopsis. Plant Physiology, 170(2), 956-970
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: 2017-11-30Bibliographically approved
Uddenberg, D., Akhter, S., Ramachandran, P., Sundström, J. F. & Carlsbecker, A. (2015). Sequenced genomes and rapidly emerging technologies pave the way for conifer evolutionary developmental biology.. Frontiers in Plant Science, 6
Open this publication in new window or tab >>Sequenced genomes and rapidly emerging technologies pave the way for conifer evolutionary developmental biology.
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2015 (English)In: Frontiers in Plant Science, ISSN 1664-462X, E-ISSN 1664-462X, Vol. 6Article in journal (Refereed) Published
Abstract [en]

Conifers, Ginkgo, cycads and gnetophytes comprise the four groups of extant gymnosperms holding a unique position of sharing common ancestry with the angiosperms. Comparative studies of gymnosperms and angiosperms are the key to a better understanding of ancient seed plant morphologies, how they have shifted over evolution to shape modern day species, and how the genes governing these morphologies have evolved. However, conifers and other gymnosperms have been notoriously difficult to study due to their long generation times, inaccessibility to genetic experimentation and unavailable genome sequences. Now, with three draft genomes from spruces and pines, rapid advances in next generation sequencing methods for genome wide expression analyses, and enhanced methods for genetic transformation, we are much better equipped to address a number of key evolutionary questions relating to seed plant evolution. In this mini-review we highlight recent progress in conifer developmental biology relevant to evo-devo questions. We discuss how genome sequence data and novel techniques might allow us to explore genetic variation and naturally occurring conifer mutants, approaches to reduce long generation times to allow for genetic studies in conifers, and other potential upcoming research avenues utilizing current and emergent techniques. Results from developmental studies of conifers and other gymnosperms in comparison to those in angiosperms will provide information to trace core molecular developmental control tool kits of ancestral seed plants, but foremost they will greatly improve our understanding of the biology of conifers and other gymnosperms in their own right.

National Category
Natural Sciences
Identifiers
urn:nbn:se:uu:diva-287677 (URN)
Available from: 2016-04-26 Created: 2016-04-26 Last updated: 2017-11-30
Ursache, R., Miyashima, S., Chen, Q., Vaten, A., Nakajima, K., Carlsbecker, A., . . . Dettmer, J. (2014). Tryptophan-dependent auxin biosynthesis is required for HD-ZIP III-mediated xylem patterning. Development, 141(6), 1250-1260
Open this publication in new window or tab >>Tryptophan-dependent auxin biosynthesis is required for HD-ZIP III-mediated xylem patterning
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2014 (English)In: Development, ISSN 0950-1991, E-ISSN 1477-9129, Vol. 141, no 6, p. 1250-1260Article in journal (Refereed) Published
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.

Keywords
Arabidopsis thaliana, Auxin biosynthesis, Metaxylem, HD-ZIP III
National Category
Biological Sciences
Identifiers
urn:nbn:se:uu:diva-222928 (URN)10.1242/dev.103473 (DOI)000332535400009 ()
Available from: 2014-04-17 Created: 2014-04-15 Last updated: 2017-12-05Bibliographically approved
Roberts, C., Valdés, A. E. & Carlsbecker, A. (2013). Class III HD-Zip transcription factors control root growth and vascular patterning. In: : . Paper presented at Plant Network Meeting, Ultuna, Uppsala, Nov 18-19, 2013..
Open this publication in new window or tab >>Class III HD-Zip transcription factors control root growth and vascular patterning
2013 (English)Conference paper, Poster (with or without abstract) (Other academic)
National Category
Biochemistry and Molecular Biology
Research subject
Biology with specialization in Physiological Botany
Identifiers
urn:nbn:se:uu:diva-213022 (URN)
Conference
Plant Network Meeting, Ultuna, Uppsala, Nov 18-19, 2013.
Available from: 2013-12-17 Created: 2013-12-17 Last updated: 2014-12-19Bibliographically approved
Roberts, C. J., Valdés, A. E. & Carlsbecker, A. (2013). Class III HD-ZIP transcription factors control root growth and vascular patterning. In: : . Paper presented at Plant Vascular Biology, Helsinki, July 26-30, 2013.
Open this publication in new window or tab >>Class III HD-ZIP transcription factors control root growth and vascular patterning
2013 (English)Conference paper, Poster (with or without abstract) (Other academic)
National Category
Biological Sciences
Identifiers
urn:nbn:se:uu:diva-214063 (URN)
Conference
Plant Vascular Biology, Helsinki, July 26-30, 2013
Available from: 2014-01-07 Created: 2014-01-07 Last updated: 2015-07-02Bibliographically approved
Valdés, A. E., Roberts, C. & Carlsbecker, A. (2013). HD-Zip class III transcription factors control root development through the modulation of ROS levels. In: : . Paper presented at 11th international POG Conference, Reactive Oxygen Species and Nitrogen Species in plants, Warsaw, July 17-19, 2013 (pp. 218-218). Committee of Biotechnology, Plish Academy of Sciences
Open this publication in new window or tab >>HD-Zip class III transcription factors control root development through the modulation of ROS levels
2013 (English)Conference paper, Oral presentation with published abstract (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.

Place, publisher, year, edition, pages
Committee of Biotechnology, Plish Academy of Sciences, 2013
Series
Biotechnologia, ISSN 0860-7796 ; 94(2)
Keywords
ROS, Plant development, HD-Zip III TFs
National Category
Biochemistry and Molecular Biology
Research subject
Biology with specialization in Physiological Botany
Identifiers
urn:nbn:se:uu:diva-213018 (URN)
Conference
11th international POG Conference, Reactive Oxygen Species and Nitrogen Species in plants, Warsaw, July 17-19, 2013
Available from: 2013-12-17 Created: 2013-12-17 Last updated: 2015-07-28Bibliographically approved
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