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Regulation of organ straightening and plant posture by an actin–myosin XI cytoskeleton

Nature Plants volume 1, Article number: 15031 (2015) Cite this article

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An Erratum to this article was published on 14 April 2015

Abstract

Plants are able to bend nearly every organ in response to environmental stimuli such as gravity and light1,2. After this first phase, the responses to stimuli are restrained by an independent mechanism, or even reversed, so that the organ will stop bending and attain its desired posture. This phenomenon of organ straightening has been called autotropism3 and autostraightening4 and modelled as proprioception5. However, the machinery that drives organ straightening and where it occurs are mostly unknown. Here, we show that the straightening of inflorescence stems is regulated by an actin–myosin XI cytoskeleton in specialized immature fibre cells that are parallel to the stem and encircle it in a thin band. Arabidopsis mutants defective in myosin XI (specifically XIf and XIk) or ACTIN8 exhibit hyperbending of stems in response to gravity, an effect independent of the physical properties of the shoots. The actin–myosin XI cytoskeleton enables organs to attain their new position more rapidly than would an oscillating series of diminishing overshoots in environmental stimuli. We propose that the long actin filaments in elongating fibre cells act as a bending tensile sensor to perceive the organ's posture and trigger the straightening system.

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Figure 1: Deficiency of myosins XIf and XIk enhances organ bending in response to gravity and light stimuli.
Figure 2: Myosins XIf and XIk are required for straightening of inflorescence stems.
Figure 3: Fibre cells expressing myosins XIf and XIk play a role in straightening.
Figure 4: Fibre cells develop extremely long actin cables and a defect in ACTIN8 causes abnormal phenotypes similar to those of myosin xif xik.

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Acknowledgements

We are grateful to Tobias Baskin (University of Massachusetts), Alistair M. Hetherington (University of Bristol) and James Raymond (Eigoken) for critical readings of this manuscript and to Moritoshi Iino (Osaka City University), Tomomi Suzuki (Kyoto University) and Akira Nagatani (Kyoto University) for helpful discussion. We are also grateful to Shoko Hongo (Tohoku University), Kazuhiko Nishitani (Tohoku University), Masatsugu Toyota (NAIST) and Masatoshi Taniguchi (NAIST) for their technical support; to Valerian V. Dolja (Oregon State University) for his donation of the ProXIk:XIk–YFP construct, transgenic seeds and anti-XIk antibody; to Takashi Ueda (University of Tokyo) for his donation of the Pro35S:Lifeact–Venus construct; to Tsuyoshi Nakagawa (Shimane University) for his donation of Gateway vectors; and to the ABRC for providing seeds of A. thaliana tDNA insertion mutants. This work was supported by Specially Promoted Research of Grant-in-Aid for Scientific Research to I.H-N. (no. 22000014), Grants-in-Aid for Scientific Research to K.O. (no. 23.2) and to H.U. (nos. 21200065 and 25440132) from the Japan Society for the Promotion of Science (JSPS).

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Author notes

  1. Keishi Okamoto and Haruko Ueda: These authors contributed equally to this work.

Authors and Affiliations

  1. Graduate School of Science, Kyoto University, Kyoto, 606-8502, Japan

    Keishi Okamoto, Haruko Ueda, Tomoo Shimada, Kentaro Tamura & Ikuko Hara-Nishimura

  2. Graduate School of Biological Sciences, Nara Institute of Science and Technology, Ikoma, 630-0101, Japan

    Takehide Kato & Masao Tasaka

  3. Graduate School of Bioagricultural Sciences, Nagoya University, Nagoya, 464-8601, Japan

    Miyo Terao Morita

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  1. Keishi Okamoto
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Contributions

K.O., H.U., T.S. and I.H-N. conceived the study; K.O. and H.U. designed the experiments; K.O. generated myosin mutants and analysed tropic responses. K.O. and H.U. generated transgenic plants and analysed straightening; K.O., T.K., M.T. and M.T.M. analysed gravitropic responses; K.O., H.U., T.S., K.T. and I.H-N. participated in discussion; K.O., H.U., T.S. and I.H-N. wrote the manuscript.

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Correspondence to Ikuko Hara-Nishimura.

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Okamoto, K., Ueda, H., Shimada, T. et al. Regulation of organ straightening and plant posture by an actin–myosin XI cytoskeleton. Nature Plants 1, 15031 (2015). https://doi.org/10.1038/nplants.2015.31

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