Tijs Ketelaar

Tip-growing cells of, amongst others, plants and fungi secrete wall materials in a highly polarized fashion for fast and efficient colonization of the environment. A polarized microtubule cytoskeleton, in which most microtubule ends are directed toward the growing apex, has been implicated in directing growth. Its organizing principles, in particular regarding maintenance of network unipolarity, have remained elusive. We show that a kinesin-4 protein, hitherto best known for a role in cytokinesis, suppresses encounters between antiparallel microtubules. Without this activity, microtubules hyper-aligned along the growth axis and increasingly grew away from the apex. Cells themselves displayed an overly straight growth path and a delayed gravitropic response. This result revealed conflicting systemic needs for a stable growth direction and an ability to change course in response to extracellular cues. Thus, the use of selective inhibition of microtubule growth at antiparallel overlaps constitutes a new organizing principle within a unipolar microtubule array.

Filamentous plant pathogens apply mechanical forces to pierce their hosts surface and penetrate its tissues. Devastating Phytophthora pathogens harness a specialized form of invasive tip growth to slice through the plant surface, wielding their hypha as a microscopic knife. Slicing requires a sharp hyphal tip that is not blunted at the site of the mechanical interaction. How tip shape is controlled, however, is unknown. We uncover an actin-based mechanostat in Phytophthora infestans that controls tip sharpness during penetration. Mechanical stimulation of the hypha leads to the emergence of an aster-like actin configuration, which shows fast, local, and quantitative feedback to the local stress. We evidence that this functions as an adaptive mechanical scaffold that sharpens the invasive weapon and prevents it from blunting. The hyphal tip mechanostat enables the efficient conversion of turgor into localized invasive pressures that are required to achieve host penetration.