Journal Article

A Mechanism for Reorientation of Cortical Microtubule Arrays Driven by Microtubule Severing

Shundyak, Kostya, Nakamura, Masayoshi, Ketelaar, Tijs, Hibbel, Anneke, Gutierrez, Ryan, Emons, Anne Mie C., Lindeboom, Jelmer J., Mulder, Bela M., Kirik, Viktor, Ehrhardt, David W.

2013

Overview

The organization of cortical microtubule arrays in higher plant cells is essential for organizing cell and tissue morphogenesis, but it is not clear how specific architectures are acquired and reconfigured in response to environmental cues. Lindeboom et al. ( 10.1126/science.1245533 , published online 7 November; see the Perspective by Roll-Mecak ) used live-cell imaging and genetic studies to show that the microtubule-severing protein, katanin, plays a crucial role in reorienting cortical arrays from transverse to longitudinal in Arabidopsis seedlings in response to blue light perception. Katanin localized to microtubule intersections where, stimulated by blue light receptors, it preferentially catalyzed the severing of the newer microtubule. The microtubule “plus” end created by severing were observed to grow preferentially, effectively building a new population of microtubules orthogonal to the initial array. The net effect of this process steers the growing seedling toward light. A self-organizing system makes the microtubule array in plants rearrange in order for the shoot to turn toward blue light. Environmental and hormonal signals cause reorganization of microtubule arrays in higher plants, but the mechanisms driving these transitions have remained elusive. The organization of these arrays is required to direct morphogenesis. We discovered that microtubule severing by the protein katanin plays a crucial and unexpected role in the reorientation of cortical arrays, as triggered by blue light. Imaging and genetic experiments revealed that phototropin photoreceptors stimulate katanin-mediated severing specifically at microtubule intersections, leading to the generation of new microtubules at these locations. We show how this activity serves as the basis for a mechanism that amplifies microtubules orthogonal to the initial array, thereby driving array reorientation. Our observations show how severing is used constructively to build a new microtubule array.

• Publisher: American Association for the Advancement of Science
• Subject: Adenosine Triphosphatases - genetics / Adenosine Triphosphatases - metabolism / Arabidopsis - genetics / Arabidopsis - growth & development / Arabidopsis - metabolism / Arabidopsis - ultrastructure / arabidopsis hypocotyl / Arabidopsis Proteins - genetics / Arabidopsis Proteins - metabolism / Arrays / Buildings / Cell growth / cell-wall / Crossovers / Epidermal cells / gamma-tubulin / Genetics / growth-rate / higher-plants / Hypocotyl - metabolism / Hypocotyl - ultrastructure / Imaging / in-vitro / Katanin / Light / maize coleoptiles / Microtubules / Microtubules - metabolism / Microtubules - ultrastructure / Online / outer epidermal wall / Perception / Phosphoproteins - metabolism / Phototropism / Plants / plasma-membrane / Proteins / Receptors / Recombinant Fusion Proteins - metabolism / RESEARCH ARTICLE SUMMARY / Retraining / Signal Transduction