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Cell-to-Cell Signalling in Arabidopsis Root Development
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Physiological Botany.
2012 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

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

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

Place, publisher, year, edition, pages
Uppsala: Acta Universitatis Upsaliensis, 2012. , 61 p.
Series
Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Science and Technology, ISSN 1651-6214 ; 979
Keyword [en]
HD-ZIP III, miRNA, plasmodesmata, auxin, ROS, xylem
National Category
Cell Biology Developmental Biology Botany
Research subject
Biology with specialization in Physiological Botany
Identifiers
URN: urn:nbn:se:uu:diva-181187ISBN: 978-91-554-8487-3 (print)OAI: oai:DiVA.org:uu-181187DiVA: diva2:558540
Public defence
2012-11-16, A281, Uppsala BioCenter, Almas Allé 5, Uppsala, 13:00 (English)
Opponent
Supervisors
Available from: 2012-10-26 Created: 2012-09-18 Last updated: 2013-01-23
List of papers
1. Cell signalling by microRNA165/6 directs gene dose-dependent root cell fate
Open this publication in new window or tab >>Cell signalling by microRNA165/6 directs gene dose-dependent root cell fate
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2010 (English)In: Nature, ISSN 0028-0836, E-ISSN 1476-4687, Vol. 465, no 7296, 316-321 p.Article in journal (Refereed) Published
Abstract [en]

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

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

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

National Category
Natural Sciences Medical and Health Sciences
Identifiers
urn:nbn:se:uu:diva-167203 (URN)10.1016/j.devcel.2011.10.006 (DOI)000298215200018 ()
Available from: 2012-01-23 Created: 2012-01-23 Last updated: 2017-12-08Bibliographically approved
3. Class III HD-ZIP Transcription Factors Determine Root Meristem Size by Controlling Reactive Oxygen Species Levels
Open this publication in new window or tab >>Class III HD-ZIP Transcription Factors Determine Root Meristem Size by Controlling Reactive Oxygen Species Levels
(English)Manuscript (preprint) (Other academic)
National Category
Botany
Identifiers
urn:nbn:se:uu:diva-181188 (URN)
Available from: 2012-10-03 Created: 2012-09-18 Last updated: 2016-04-25
4. Class III HD-ZIP Transcription Factors Regulate Auxin Signalling to Pattern Arabidopsis Root Vasculature
Open this publication in new window or tab >>Class III HD-ZIP Transcription Factors Regulate Auxin Signalling to Pattern Arabidopsis Root Vasculature
(English)Manuscript (preprint) (Other academic)
National Category
Botany
Identifiers
urn:nbn:se:uu:diva-181189 (URN)
Available from: 2012-10-03 Created: 2012-09-18 Last updated: 2016-04-25

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