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Patterning mechanisms of cytoskeletal and cell wall systems during leaf trichome morphogenesis

Nature Plants volume 1, Article number: 15014 (2015) Cite this article

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Abstract

The plant actin cytoskeleton is an unstable network of filaments that influences polarized growth through poorly understood mechanisms. Here, we used a combination of live cell imaging and finite element computational modelling of Arabidopsis trichome morphogenesis to determine how the actin and microtubule cytoskeletons cooperate to pattern the cell wall and growth. The actin-related protein (ARP)2/3 complex generates an actin meshwork that operates within a tip-localized, microtubule-depleted zone to modulate cell wall anisotropy locally. The actin meshwork also positions an actin bundle network that organizes organelle flow patterns. This activity is required to maintain cell wall thickness gradients that enable tip-biased diffuse growth. These newly discovered couplings between cytoskeletal patterns and wall textures provide important insights into the cellular mechanism of growth control in plants.

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Figure 1: The geometry of trichome shape change and cell wall strain.
Figure 2: Finite element model of trichome branch morphogenesis.
Figure 3: Growth and cell wall analysis of an ARP2/3 null mutant.
Figure 4: ARP2/3 generates apical actin meshworks within the microtubule-depletion zone.

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Acknowledgements

We thank David Umulis for helpful discussions. Thanks to Adam Fessenden for reflected light time-lapse imaging. We also thank Chia-Ping Huang and the Purdue Life Science Microscopy Facility for their expert assistance. This research was supported by NSF Grant IOS Grant No. 1249652 to D.B.S and J.A.T. and NSF MCB Grant No. 1121893 to D.B.S.

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Authors and Affiliations

  1. Department of Botany and Plant Pathology, Purdue University, West Lafayette, 47907, Indiana, USA

    Makoto Yanagisawa, Samuel A. Belteton, Eileen L. Mallery & Daniel B. Szymanski

  2. Department of Mechanical and Materials Engineering, University of Nebraska-Lincoln, Lincoln, 68588, Nebraska, USA

    Anastasia S. Desyatova & Joseph A. Turner

  3. Biological Sciences, Purdue University, West Lafayette, 47907, Indiana, USA

    Daniel B. Szymanski

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  1. Makoto Yanagisawa
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Contributions

All authors participated in the experimental design, data collection, data analysis and manuscript preparation. D.S. conceived the project. J.T. and A.D. developed the finite element models. S.B. did the reflected light and TEM analyses. E.M. created the ARP2/3–GFP live-cell probe. M.Y. conducted all other wet laboratory experiments.

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Correspondence to Daniel B. Szymanski.

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Yanagisawa, M., Desyatova, A., Belteton, S. et al. Patterning mechanisms of cytoskeletal and cell wall systems during leaf trichome morphogenesis. Nature Plants 1, 15014 (2015). https://doi.org/10.1038/nplants.2015.14

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