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PMID:20807878

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Citation

Khurana, P, Henty, JL, Huang, S, Staiger, AM, Blanchoin, L and Staiger, CJ (2010) Arabidopsis VILLIN1 and VILLIN3 have overlapping and distinct activities in actin bundle formation and turnover. Plant Cell 22:2727-48

Abstract

Actin filament bundles are higher-order cytoskeletal structures that are crucial for the maintenance of cellular architecture and cell expansion. They are generated from individual actin filaments by the actions of bundling proteins like fimbrins, LIMs, and villins. However, the molecular mechanisms of dynamic bundle formation and turnover are largely unknown. Villins belong to the villin/gelsolin/fragmin superfamily and comprise at least five isovariants in Arabidopsis thaliana. Different combinations of villin isovariants are coexpressed in various tissues and cells. It is not clear whether these isovariants function together and act redundantly or whether they have unique activities. VILLIN1 (VLN1) is a simple filament-bundling protein and is Ca(2+) insensitive. Based on phylogenetic analyses and conservation of Ca(2+) binding sites, we predict that VLN3 is a Ca(2+)-regulated villin capable of severing actin filaments and contributing to bundle turnover. The bundling activity of both isovariants was observed directly with time-lapse imaging and total internal reflection fluorescence (TIRF) microscopy in vitro, and the mechanism mimics the "catch and zipper" action observed in vivo. Using time-lapse TIRF microscopy, we observed and quantified the severing of individual actin filaments by VLN3 at physiological calcium concentrations. Moreover, VLN3 can sever actin filament bundles in the presence of VLN1 when calcium is elevated to micromolar levels. Collectively, these results demonstrate that two villin isovariants have overlapping and distinct activities.

Links

PubMed PMC2947172 Online version:10.1105/tpc.110.076240

Keywords

Actins/biosynthesis; Arabidopsis/genetics; Arabidopsis/metabolism; Arabidopsis Proteins/genetics; Arabidopsis Proteins/metabolism; Binding Sites; Calcium/metabolism; Microfilament Proteins/genetics; Microfilament Proteins/metabolism; Protein Isoforms/genetics; Protein Isoforms/metabolism

Significance

Annotations

Gene product Qualifier GO Term Evidence Code with/from Aspect Extension Notes Status

ARATH:VILI3

acts_upstream_of_or_within

GO:0051017: actin filament bundle assembly

ECO:0000314: direct assay evidence used in manual assertion

P

Seeded From UniProt

complete

ARATH:VILI3

acts_upstream_of_or_within

GO:0051014: actin filament severing

ECO:0000314: direct assay evidence used in manual assertion

P

Seeded From UniProt

complete

ARATH:VILI3

enables

GO:0051015: actin filament binding

ECO:0000314: direct assay evidence used in manual assertion

F

Seeded From UniProt

complete

ORYSJ:VLN1

NOT|involved_in

GO:0051592: response to calcium ion

ECO:0000314: direct assay evidence used in manual assertion

P

Seeded From UniProt

complete

ORYSJ:VLN1

NOT|involved_in

GO:0051014: actin filament severing

ECO:0000314: direct assay evidence used in manual assertion

P

Seeded From UniProt

complete

ORYSJ:VLN1

enables

GO:0051015: actin filament binding

ECO:0000314: direct assay evidence used in manual assertion

F

Seeded From UniProt

complete

ORYSJ:VLN3

involved_in

GO:0007015: actin filament organization

ECO:0000314: direct assay evidence used in manual assertion

P

Seeded From UniProt

complete

ORYSJ:VLN3

located_in

GO:0032432: actin filament bundle

ECO:0000314: direct assay evidence used in manual assertion

C

Seeded From UniProt

complete

ORYSJ:VLN3

involved_in

GO:0051693: actin filament capping

ECO:0000314: direct assay evidence used in manual assertion

P

Seeded From UniProt

complete

ORYSJ:VLN3

involved_in

GO:0051592: response to calcium ion

ECO:0000314: direct assay evidence used in manual assertion

P

Seeded From UniProt

complete

ORYSJ:VLN3

involved_in

GO:0051014: actin filament severing

ECO:0000314: direct assay evidence used in manual assertion

P

Seeded From UniProt

complete

ORYSJ:VLN3

enables

GO:0051015: actin filament binding

ECO:0000314: direct assay evidence used in manual assertion

F

Seeded From UniProt

complete


See also

References

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