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- Title
Microtubule associated protein WAVE DAMPENED2-LIKE (WDL) controls microtubule bundling and the stability of the site of tip-growth in Marchantia polymorpha rhizoids.
- Authors
Champion, Clement; Lamers, Jasper; Jones, Victor Arnold Shivas; Morieri, Giulia; Honkanen, Suvi; Dolan, Liam
- Abstract
Tip-growth is a mode of polarized cell expansion where incorporation of new membrane and wall is stably restricted to a single, small domain of the cell surface resulting in the formation of a tubular projection that extends away from the body of the cell. The organization of the microtubule cytoskeleton is conserved among tip-growing cells of land plants: bundles of microtubules run longitudinally along the non-growing shank and a network of fine microtubules grow into the apical dome where growth occurs. Together, these microtubule networks control the stable positioning of the growth site at the cell surface. This conserved dynamic organization is required for the spatial stability of tip-growth, as demonstrated by the formation of sinuous tip-growing cells upon treatment with microtubule-stabilizing or microtubule-destabilizing drugs. Microtubule associated proteins (MAPs) that either stabilize or destabilize microtubule networks are required for the maintenance of stable tip-growth in root hairs of flowering plants. NIMA RELATED KINASE (NEK) is a MAP that destabilizes microtubule growing ends in the apical dome of tip-growing rhizoid cells in the liverwort Marchantia polymorpha. We hypothesized that both microtubule stabilizing and destabilizing MAPs are required for the maintenance of the stable tip-growth in liverworts. To identify genes encoding microtubule-stabilizing and microtubule-destabilizing activities we generated 120,000 UV-B mutagenized and 336,000 T-DNA transformed Marchantia polymorpha plants and screened for defective rhizoid phenotypes. We identified 119 mutants and retained 30 mutants in which the sinuous rhizoid phenotype was inherited. The 30 mutants were classified into at least 4 linkage groups. Characterisation of two of the linkage groups showed that MAP genes–WAVE DAMPENED2-LIKE (WDL) and NIMA-RELATED KINASE (NEK)–are required to stabilize the site of tip growth in elongating rhizoids. Furthermore, we show that MpWDL is required for the formation of a bundled array of parallel and longitudinally orientated microtubules in the non-growing shank of rhizoids where MpWDL-YFP localizes to microtubule bundles. We propose a model where the opposite functions of MpWDL and MpNEK on microtubule bundling are spatially separated and promote tip-growth spatial stability. Author summary: Plant cells control where they grow by adding membrane and cell wall material to a defined area of their surface. In particular, filamentous rooting cells develop the cellular projections essential to their function by restricting cell expansion to a stable domain of their surface. The spatial stability of this mechanism known as tip-growth defines the final shape of the cellular projections–straight projections form from stable tip-growth, while wavy or bifurcating projections form from unstable tip-growth. Microtubules are known to regulate tip-growth stability. Both microtubule stabilisation and destabilisation leads to unstable tip-growth. We have discovered two proteins that associate with microtubules, control their stability and are required for stabilizing tip-growth in the common liverwort. The first protein is known to destabilize microtubules in the tip of filamentous rooting cells of the common liverwort, and we found the second protein to stabilize, or bundle, microtubules in their shank. This is important because it is the first protein found to stabilize microtubules in the common liverwort and because it is the first time a protein stabilizing microtubules in rooting cells of plants is shown to localize separately from proteins that destabilizes microtubules. We propose that tip-growth stability requires the opposite functions of these two microtubule associated protein to be spatially separated.
- Subjects
MICROTUBULE-associated proteins; MICROTUBULES; TUBULINS; RHIZOIDS; PLANT microtubules; FLOWERING of plants
- Publication
PLoS Genetics, 2021, Vol 17, Issue 6, p1
- ISSN
1553-7390
- Publication type
Article
- DOI
10.1371/journal.pgen.1009533