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Cell–cell adhesion in plant grafting is facilitated by β-1,4-glucanases

View ORCID ProfileMichitaka Notaguchi, Ken-ichi Kurotani, Yoshikatsu Sato, Ryo Tabata, Yaichi Kawakatsu, Koji Okayasu, Yu Sawai, Ryo Okada, Masashi Asahina, Yasunori Ichihashi, View ORCID ProfileKen Shirasu, Takamasa Suzuki, Masaki Niwa, Tetsuya Higashiyama
doi: https://doi.org/10.1101/2020.03.26.010744
Michitaka Notaguchi
1Bioscience and Biotechnology Center, Nagoya University, Furo-cho, Chikusa-ku, Nagoya 464-8601, Japan
2Graduate School of Bioagricultural Sciences, Nagoya University, Furo-cho, Chikusa-ku, Nagoya 464-8601, Japan
3Institute of Transformative Bio-Molecules, Nagoya University, Furo-cho, Chikusa-ku, Nagoya 464-8601, Japan
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  • ORCID record for Michitaka Notaguchi
  • For correspondence: notaguchi.michitaka@b.mbox.nagoya-u.ac.jp
Ken-ichi Kurotani
1Bioscience and Biotechnology Center, Nagoya University, Furo-cho, Chikusa-ku, Nagoya 464-8601, Japan
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Yoshikatsu Sato
3Institute of Transformative Bio-Molecules, Nagoya University, Furo-cho, Chikusa-ku, Nagoya 464-8601, Japan
4Graduate School of Science, Nagoya University, Furo-cho, Chikusa-ku, Nagoya 464-8601, Japan
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Ryo Tabata
2Graduate School of Bioagricultural Sciences, Nagoya University, Furo-cho, Chikusa-ku, Nagoya 464-8601, Japan
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Yaichi Kawakatsu
2Graduate School of Bioagricultural Sciences, Nagoya University, Furo-cho, Chikusa-ku, Nagoya 464-8601, Japan
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Koji Okayasu
2Graduate School of Bioagricultural Sciences, Nagoya University, Furo-cho, Chikusa-ku, Nagoya 464-8601, Japan
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Yu Sawai
2Graduate School of Bioagricultural Sciences, Nagoya University, Furo-cho, Chikusa-ku, Nagoya 464-8601, Japan
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Ryo Okada
2Graduate School of Bioagricultural Sciences, Nagoya University, Furo-cho, Chikusa-ku, Nagoya 464-8601, Japan
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Masashi Asahina
5Department of Biosciences, Teikyo University, Utsunomiya, Tochigi 320-8551, Japan
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Yasunori Ichihashi
6Center for Sustainable Resource Science, RIKEN, Tsurumi, Yokohama, Kanagawa 230-0045, Japan
7RIKEN BioResource Research Center, Tsukuba, Ibaraki 305-0074, Japan
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Ken Shirasu
6Center for Sustainable Resource Science, RIKEN, Tsurumi, Yokohama, Kanagawa 230-0045, Japan
8Graduate School of Science, The University of Tokyo, Hongo, Bunkyo-ku, Tokyo 113-0033, Japan
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Takamasa Suzuki
9College of Bioscience and Biotechnology, Chubu University, Matsumoto-cho, Kasugai 487-8501, Japan
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Masaki Niwa
2Graduate School of Bioagricultural Sciences, Nagoya University, Furo-cho, Chikusa-ku, Nagoya 464-8601, Japan
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Tetsuya Higashiyama
3Institute of Transformative Bio-Molecules, Nagoya University, Furo-cho, Chikusa-ku, Nagoya 464-8601, Japan
4Graduate School of Science, Nagoya University, Furo-cho, Chikusa-ku, Nagoya 464-8601, Japan
8Graduate School of Science, The University of Tokyo, Hongo, Bunkyo-ku, Tokyo 113-0033, Japan
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Abstract

Plant grafting is conducted for vegetative propagation in plants, whereby a piece of living tissue is attached to another tissue through establishment of cell–cell adhesion. Plant grafting has a long history in agriculture and has been applied to improve crop traits for thousands of years1. Plant grafting has mostly relied on the natural ability of a plant for wound healing. However, the compatibility of cell–cell adhesion typically limits graft combinations to closely related species2–4, and the mechanism by which cell–cell adhesion of injured tissues is established is largely unknown. Here, we show that a subclade of β-1,4-glucanases secreted into the extracellular region facilitates cell–cell adhesion near the graft interface. Nicotiana shows a propensity for cell–cell adhesion with a diverse range of angiosperms, including vegetables, fruit trees, and monocots, in which cell wall reconstruction was promoted in a similar manner to conventional intrafamily grafting5–7. Using transcriptomic approaches, we identified a specific clade of β-1,4-glucanases that is upregulated during grafting in successful graft combinations but not in incompatible grafts and precedes graft adhesion in inter- and intrafamily grafts. Grafting was facilitated with an overexpressor of the β-1,4-glucanase and, using Nicotiana stem as an interscion, we produced tomato fruits on rootstocks from other plant families. Our results demonstrate that the mechanism of cell–cell adhesion is partly conserved in plants and is a potential target to enhance plant grafting techniques.

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Posted March 29, 2020.
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Cell–cell adhesion in plant grafting is facilitated by β-1,4-glucanases
Michitaka Notaguchi, Ken-ichi Kurotani, Yoshikatsu Sato, Ryo Tabata, Yaichi Kawakatsu, Koji Okayasu, Yu Sawai, Ryo Okada, Masashi Asahina, Yasunori Ichihashi, Ken Shirasu, Takamasa Suzuki, Masaki Niwa, Tetsuya Higashiyama
bioRxiv 2020.03.26.010744; doi: https://doi.org/10.1101/2020.03.26.010744
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Cell–cell adhesion in plant grafting is facilitated by β-1,4-glucanases
Michitaka Notaguchi, Ken-ichi Kurotani, Yoshikatsu Sato, Ryo Tabata, Yaichi Kawakatsu, Koji Okayasu, Yu Sawai, Ryo Okada, Masashi Asahina, Yasunori Ichihashi, Ken Shirasu, Takamasa Suzuki, Masaki Niwa, Tetsuya Higashiyama
bioRxiv 2020.03.26.010744; doi: https://doi.org/10.1101/2020.03.26.010744

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