The genetic control of microtubule-mediated tip-growth stability in the liverwort Marchantia polymorpha

Polar growth is an important mechanism for plant cell morphogenesis. Tip-growth represents an extreme mode of polar growth where cell expansion is stably restricted to a narrow domain of the cell periphery resulting in the formation of a tubular cell projection. The microtubule cytoskeleton controls the stable positioning of the growth region in tip-growing cells of flowering plants and mosses. I show that this holds true in the earliest diverging clade of land plants, the liverworts. In Marchantia polymorpha, pharmacological destabilization of the microtubule cytoskeleton leads to the formation of wavy or bifurcating rhizoids, a tip-growing cell type analogous to root hairs of flowering plants and to caulonema cells of mosses. Characterization of the organisation of the microtubule cytoskeleton in growing rhizoids of Marchantia polymorpha revealed longitudinally oriented microtubules that grow towards and converge into the apical dome. Because microtubule-associated proteins (MAPs) control the organisation of the microtubule cytoskeleton I generated the first de novo genome assembly of Marchantia polymorpha and compared the MAP repertoire of the liverwort model with that of existing model organisms of the green lineage. A mutant screen in Marchantia polymorpha identified the function of MpWAVE DAMPENED LIKE (MpWDL) and MpNIMA-RELATED KINASE (MpNEK) in microtubule-mediated tip-growth stability. MpWDL localizes preferentially to microtubules in the shank of growing rhizoids, where it promotes the longitudinal orientation of the microtubule cytoskeleton. These results are discussed in the context of the evolution of microtubule-mediated tip-growth stability and the tentative hypothesis that the underlying mechanism differs between flowering plants and bryophytes is proposed.