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Arabidopsis SABRE and CLASP interact to stabilize cell division plane orientation and planar polarity
Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
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2013 (English)In: Nature Communications, ISSN 2041-1723, E-ISSN 2041-1723, Vol. 4, 2779- p.Article in journal (Refereed) Published
Abstract [en]

The orientation of cell division and the coordination of cell polarity within the plane of the tissue layer (planar polarity) contribute to shape diverse multicellular organisms. The root of Arabidopsis thaliana displays regularly oriented cell divisions, cell elongation and planar polarity providing a plant model system to study these processes. Here we report that the SABRE protein, which shares similarity with proteins of unknown function throughout eukaryotes, has important roles in orienting cell division and planar polarity. SABRE localizes at the plasma membrane, endomembranes, mitotic spindle and cell plate. SABRE stabilizes the orientation of CLASP-labelled preprophase band microtubules predicting the cell division plane, and of cortical microtubules driving cell elongation. During planar polarity establishment, sabre is epistatic to clasp at directing polar membrane domains of Rho-of-plant GTPases. Our findings mechanistically link SABRE to CLASP-dependent microtubule organization, shedding new light on the function of SABRE-related proteins in eukaryotes.

Place, publisher, year, edition, pages
Nature Publishing Group, 2013. Vol. 4, 2779- p.
National Category
Botany
Identifiers
URN: urn:nbn:se:umu:diva-85312DOI: 10.1038/ncomms3779ISI: 000328023900017OAI: oai:DiVA.org:umu-85312DiVA: diva2:693921
Funder
Swedish Research Council, 2006-522, 2009-4846Knut and Alice Wallenberg Foundation
Available from: 2014-02-05 Created: 2014-01-31 Last updated: 2017-12-06Bibliographically approved
In thesis
1. Characterization of New Players in Planar Polarity Establishment in Arabidopsis
Open this publication in new window or tab >>Characterization of New Players in Planar Polarity Establishment in Arabidopsis
2014 (English)Doctoral thesis, comprehensive summary (Other academic)
Alternative title[sv]
Karakterisering av nya aktörer vid etablering av planpolaritet i Arabidopsis
Abstract [en]

Coordinated polarity and differentiation of cells in the plane of a tissue layer are essential to the development of multicellular organisms. Arabidopsis thaliana root hairs and trichomes provide model systems to study the pathways that control planar polarity and cell fate specification in plants. A concentration gradient of the plant hormone auxin provides an instructive cue that coordinates polar assembly of signalling complexes at plasma membranes of root epidermal cells; however, knowledge about additional players and cytoskeletal effectors driving cell polarization prior to hair emergence remains limited. On the other hand, epidermal cell fate specification is controlled by a well-characterized gene network of transcription factors that translate positional signals and cell-to-cell communication into tissue-wide patterning. Yet, new components are continuously found to interact with the patterning pathway, shedding light on its connections with diverse developmental processes.

This thesis presents the SABRE (SAB) gene as a novel player in planar polarity establishment and root epidermal patterning. SAB is a large protein with sequence similarity to proteins present in all eukaryotes and affects planar polarity as well as orientation of cell divisions and cortical microtubules. Genetic interaction with the microtubule-associated protein gene CLASP further supports involvement of SAB in microtubule arrangement, suggesting a role for this gene in cytoskeletal organisation. Strikingly, SAB also interacts genetically with ACTIN7 (ACT7), and both ACT7 and its modulator ACTIN INTERACTING PROTEIN 1-2 (AIP1-2) contribute to planar polarity of root hair positioning. Cell-file specific expression of AIP1-2 depends on the epidermal-patterning regulator WEREWOLF (WER), revealing a connection between actin organization, planar polarity and cell fate specification. Consistent with this finding, SAB also functions in patterning of the root epidermis by stabilizing cell fate acquisition upstream of the core patterning pathway. These results unveil new roles for SAB in planar polarity and epidermal patterning and suggest that organization of the microtubule and the actin cytoskeleton are important to both planar polarity establishment and cell fate specification.

Abstract [sv]

Samordning av polaritet och differentiering av celler inom ett vävnadslager är avgörande för utvecklingen av multicellulära organismer. Rothår och bladhår hos Arabidopsis thaliana utgör modellsystem för att studera signalvägar som kontrollerar planpolaritet och specifikation av cellers öde hos växter. En koncentrationsgradient av växthormonet auxin ger en instruktiv signal som koordinerar polär hopsättning av signalkomplex vid plasmamembranet i rotepidermisceller; dock är kunskapen om ytterligare aktörer och hur cytoskelettets aktörer påverkar cellpolaritet innan rothår bildas begränsad. Vad gäller differentieringen av epidermala cellers öde kontrolleras dessa genom ett väl karakteriserat nätverk av transkriptionsfaktorer som överför positionssignaler och cell-till-cell kommunikation till vävnadsomfattande mönsterbildning. Fortfarande hittas dock nya komponenter som interagerar med signalvägarna för mönsterbildning, vilket ger nya insikter om dess förbindelser med diverse utvecklingsprocesser.

Denna avhandling presenterar genen SABRE (SAB) som en ny aktör i etableringen av planpolaritet och mönsterbildning av rotepidermis. SAB är ett stort protein som har sekvenslikhet med proteiner som finns i alla eukaryoter och det påverkar planpolaritet, orientering av celldelning och kortikala mikrotubler. Genetisk interaktion med genen för det mikrotubuli-associerade proteinet CLASP stärker ytterligare inblandningen av SAB i organiserandet av mikrotubler och antyder att denna gen har en roll i organiserandet av cytoskelettet. Slående är att SAB även interagerar genetiskt med ACTIN7 (ACT7) och att både ACT7 och dess modulator ACTIN-INTERACTING PROTEIN1-2 (AIP1-2) bidrar till planpolaritet vid positionering av rothår. Cellfils-specifikt uttryck av AIP1-2 beror på den epidermala mönsterbildande genen WEREWOLF (WER), vilket påvisar ett samband mellan organisationen av aktin, planpolaritet och specifikationen av cellers öde. SAB fungerar även i mönsterbildning av rotens epidermis och stabiliserar förvärvet av cellöde uppströms av den centrala signalvägen för mönsterbildning. Dessa resultat visar på nya roller för SAB i planpolaritet och mönsterbildning av epidermis och indikerar att organiseringen av mikrotubler och aktin-cytoskelettet är viktiga både för etablerandet av planpolaritet och för specificeringen av cellers öde.

Place, publisher, year, edition, pages
Umeå: Umeå University, 2014. 71 p.
Keyword
SABRE, planar polarity, CLASP, cell division orientation, microtubule cytoskeleton, actin, AIP1, patterning
National Category
Developmental Biology Cell Biology
Research subject
Developmental Biology
Identifiers
urn:nbn:se:umu:diva-87838 (URN)978-91-7601-050-1 (ISBN)
Public defence
2014-05-09, KBC huset, Stora hörsalen KB3B1, Umeå universitet, Umeå, 10:00 (English)
Opponent
Supervisors
Available from: 2014-04-17 Created: 2014-04-11 Last updated: 2015-02-26Bibliographically approved
2. Characterisation of actin cytoskeletal functions and interactions during planar polarity formation in Arabidopsis
Open this publication in new window or tab >>Characterisation of actin cytoskeletal functions and interactions during planar polarity formation in Arabidopsis
2014 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

The establishment of cell and tissue polarity is essential for the development of eukaryotic organisms including plants and animals. When cell polarity is uniformly organised within a plane of a single tissue layer, it is referred to as planar polarity. In the model plant Arabidopsis thaliana, the polarly organised formation of root hairs towards the basal (root tip-oriented) ends of epidermal cells provides an ideal model system to study planar polarity formation. The instructive cue which uniformly organises tissue polarity in the Arabidopsis root epidermis is a concentration gradient of the plant hormone auxin. This concentration gradient leads to the polar recruitment of Rho-of-plant proteins to membrane sites where root hairs will form, making them the earliest cellular markers of planar polarity. Despite having identified several of the components required for planar polarity formation and the cellular read-out of it, little is known about how planar polarity is perceived and stably executed on the single cell level. Recently, a role for ACTIN2 in polar hair positioning was described, suggesting that actin may be involved in the cellular read-out of planar polarity.

In the work presented here, we further investigate the contribution of the actin cytoskeleton to polar hair positioning. We identify a role for actin upstream of polar Rho-of-plant (ROP) positioning and describe ACTIN7 and ACTIN-INTERACTING PROTEIN1-2 (AIP1-2) as components required for planar polarity formation which interact directly in yeast and in vitro and genetically during planar polarity formation. AIP1-2 expression proves hair cell file-specific and depends on WEREWOLF function, revealing a link between planar polarity and cell fate patterning in the root. In addition we find that ACT7 genetically interacts with SABRE (SAB) and that actin and SAB co-localise at the cell plate and plasma membrane domains during cell division. Furthermore, we show that actin is not only involved in the positioning, but also in the organisation of the polar membrane domain which marks where a root hair will form. Among the components which localise at this site are the phosphoinositide-biosynthetic enzyme PHOSPHATIDYLINOSITOL 4-PHOSPHATE 5-KINASE3 (PIP5K3), the DYNAMIN-RELATED PROTEINs (DRPs) DRP1A and DRP2B, the D6 PROTEIN KINASE (D6PK) and membrane sterols. For several of these components, we report a function in planar polarity formation and in the organisation of the hair initiation site.

With this work, we provide deeper insight into the function of the actin cytoskeleton and its interactions during planar polarity formation and identify additional components that contribute to the process. Moreover, we report AIP1-2 placement under control of the cell fate patterning system during establishment of planar polarity. Our results provide stepping stones for future studies aimed at investigating the mechanistic processes that contribute to planar polarity formation in more molecular and cellular detail.

Place, publisher, year, edition, pages
Umeå: Umeå universitet, 2014. 75 p.
National Category
Botany
Identifiers
urn:nbn:se:umu:diva-93023 (URN)978-91-7601-133-1 (ISBN)
Public defence
2014-10-10, Biologihuset, BiA201, Umeå Universitet, Umeå, 10:00 (English)
Opponent
Supervisors
Available from: 2014-09-19 Created: 2014-09-10 Last updated: 2015-05-07Bibliographically approved

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Pietra, StefanoGustavsson, AnnaKiefer, ChristianKalmbach, LotharHörstedt, PerIkeda, YoshihisaGrebe, Markus
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