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Characterisation of actin cytoskeletal functions and interactions during planar polarity formation in Arabidopsis
Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC). (Markus Grebe)
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: urn:nbn:se:umu:diva-93023ISBN: 978-91-7601-133-1 (print)OAI: oai:DiVA.org:umu-93023DiVA: diva2:745458
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
List of papers
1. 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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2015 (English)In: Development, ISSN 0950-1991, E-ISSN 1477-9129, Vol. 142, no 1, 151-161 p.Article in journal (Refereed) Published
Abstract [en]

The coordination of cell polarity within the plane of the tissue layer (planar polarity) is crucial for the development of diverse multicellular organisms. Small Rac/Rho-family GTPases and the actin cytoskeleton contribute to planar polarity formation at sites of polarity establishment in animals and plants. Yet, upstream pathways coordinating planar polarity differ strikingly between kingdoms. In the root of Arabidopsis thaliana, a concentration gradient of the phytohormone auxin coordinates polar recruitment of Rho-of-plant (ROP) to sites of polar epidermal hair initiation. However, little is known about cytoskeletal components and interactions that contribute to this planar polarity or about their relation to the patterning machinery. Here, we show that ACTIN7 (ACT7) represents a main actin isoform required for planar polarity of root hair positioning, interacting with the negative modulator ACTIN-INTERACTING PROTEIN1-2 (AIP1-2). ACT7, AIP1-2 and their genetic interaction are required for coordinated planar polarity of ROP downstream of ethylene signalling. Strikingly, AIP1-2 displays hair cell file-enriched expression, restricted by WEREWOLF (WER)-dependent patterning and modified by ethylene and auxin action. Hence, our findings reveal AIP1-2, expressed under control of the WER-dependent patterning machinery and the ethylene signalling pathway, as a modulator of actin-mediated planar polarity.

Keyword
AIP1, Arabidopsis, WEREWOLF, Actin, Patterning, Planar polarity
National Category
Botany
Identifiers
urn:nbn:se:umu:diva-100147 (URN)10.1242/dev.111013 (DOI)000348240500020 ()25428588 (PubMedID)
Funder
Swedish Research Council, 2003-2744
Available from: 2015-02-26 Created: 2015-02-24 Last updated: 2017-12-04Bibliographically approved
2. 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, 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
National Category
Botany
Identifiers
urn:nbn:se:umu:diva-85312 (URN)10.1038/ncomms3779 (DOI)000328023900017 ()
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
3. D6PK AGCVIII kinase is a lipid domain-dependent mediator of Arabidopsis planar polarity
Open this publication in new window or tab >>D6PK AGCVIII kinase is a lipid domain-dependent mediator of Arabidopsis planar polarity
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(English)Manuscript (preprint) (Other academic)
National Category
Botany
Identifiers
urn:nbn:se:umu:diva-92856 (URN)
Available from: 2014-09-07 Created: 2014-09-07 Last updated: 2015-02-26Bibliographically approved

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