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Characterization of New Players in Planar Polarity Establishment in Arabidopsis
2014 (English)Doctoral thesis, comprehensive summary (Other academic)
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, pages
Umeå: Umeå University, 2014. 71 p.
Keyword [en]
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)oai:DiVA.org:umu-87838 (OAI)diva2:711983 (DiVA)
Public defence
2014-05-09, KBC huset, Stora hörsalen KB3B1, Umeå universitet, Umeå, 10:00 (English)
Opponent
Supervisors
Available from2014-04-17 Created:2014-04-11 Last updated:2014-04-14Bibliographically approved
List of papers
1. Arabidopsis SABRE and CLASP interact to stabilize cell division plane orientation and planar polarity
Open this publication in new window or tab >>Arabidopsis SABRE and CLASP interact to stabilize cell division plane orientation and planar polarity
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2013 (English)In: Nature Communications, ISSN 2041-1723, Vol. 4, 2779-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.

Publisher, range
Nature Publishing Group, 2013
National Category
Botany
Identifiers
urn:nbn:se:umu:diva-85312 (URN)10.1038/ncomms3779 (DOI)000328023900017 ()
Funder
Swedish Research CouncilKnut and Alice Wallenberg Foundation
Available from2014-02-05 Created:2014-01-31 Last updated:2014-09-11Bibliographically approved
2. Arabidopsis AIP1-2 restricted by WER-mediated patterning modulates planar polarity
Open this publication in new window or tab >>Arabidopsis AIP1-2 restricted by WER-mediated patterning modulates planar polarity
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(English)Manuscript (preprint) (Other academic)
National Category
Cell Biology Developmental Biology
Research subject
Developmental Biology
Identifiers
urn:nbn:se:umu:diva-87836 (URN)
Funder
Swedish Research Council
Available from2014-04-11 Created:2014-04-11 Last updated:2014-09-11Bibliographically approved
3. SABRE is required for stabilization of root hair patterning in Arabidopsis thaliana
Open this publication in new window or tab >>SABRE is required for stabilization of root hair patterning in Arabidopsis thaliana
(English)Manuscript (preprint) (Other academic)
National Category
Developmental Biology Cell Biology
Research subject
Developmental Biology
Identifiers
urn:nbn:se:umu:diva-87837 (URN)
Funder
Swedish Research Council
Available from2014-04-11 Created:2014-04-11 Last updated:2014-04-17Bibliographically approved

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Pietra, Stefano
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