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Antagonistic regulation of the gibberellic acid response during stem growth in rice

Nagai, Keisuke Mori, Yoshinao Ishikawa, Shin Furuta, Tomoyuki Gamuyao, Rico Niimi, Yoko Hobo, Tokunori Fukuda, Moyuri Kojima, Mikiko Takebayashi, Yumiko Fukushima, Atsushi Himuro, Yasuyo Kobayashi, Masatomo Ackley, Wataru Hisano, Hiroshi Sato, Kazuhiro Yoshida, Aya Wu, Jianzhong Sakakibara, Hitoshi Sato, Yutaka Tsuji, Hiroyuki Akagi, Takashi Ashikari, Motoyuki 名古屋大学

2020.08.06

概要

The size of plants is largely determined by growth of the stem. Stem elongation is stimulated by gibberellic acid1,2,3. Here we show that internode stem elongation in rice is regulated antagonistically by an ‘accelerator’ and a ‘decelerator’ in concert with gibberellic acid. Expression of a gene we name ACCELERATOR OF INTERNODE ELONGATION 1 (ACE1), which encodes a protein of unknown function, confers cells of the intercalary meristematic region with the competence for cell division, leading to internode elongation in the presence of gibberellic acid. By contrast, upregulation of DECELERATOR OF INTERNODE ELONGATION 1 (DEC1), which encodes a zinc-finger transcription factor, suppresses internode elongation, whereas downregulation of DEC1 allows internode elongation. We also show that the mechanism of internode elongation that is mediated by ACE1 and DEC1 is conserved in the Gramineae family. Furthermore, an analysis of genetic diversity suggests that mutations in ACE1 and DEC1 have historically contributed to the selection of shorter plants in domesticated populations of rice to increase their resistance to lodging, and of taller plants in wild species of rice for adaptation to growth in deep water. Our identification of these antagonistic regulatory factors enhances our understanding of the gibberellic acid response as an additional mechanism that regulates internode elongation and environmental fitness, beyond biosynthesis and gibberellic acid signal transduction.

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Acknowledgments: We thank Prof. Hiroko Morishima (deceased 2010) for encouragement to do this

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work and Kensuke Suzuki, Yuma Kondo, Masaya Koike, Anzu Minami, Stefan Reuscher, Naoki

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Yamaji, Jian Feng Ma and Sayaka Sasaki for technical assistance. We thank Masafumi Mikami,

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Funding: This work was supported by the CREST program of the JST (no. JPMJCR13B1), by the

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SATREPS program (no. JPMJSA1706) of the JST and JICA, and by MEXT/JSPS KAKENHI (nos.

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16K18565, 16H06466, 17H06473, and 19K15815). This study was supported in part by RIKEN-

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Nagoya University Science and Technology Hub.

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Authors’ contributions: K.N. and M.A. designed the study. K.N. and S.I. carried out the genetic

1191

linkage analysis. J.W. and T.F. performed the screening of bacterial artificial chromosome clones and

1192

sequence analysis. K.N., R.G., Y.N., M.F., Y.H., M.K., W.A., H.H., and K.S. performed the transgenic

1193

experiments and sequence analysis. K.N., Y.M., R.G., T.H., A.Y., and H.T. elucidated the molecular

1194

mechanisms. M.K., Y.T., and H.S. quantified the hormone levels. A.F. performed the trans-eQTL

1195

analysis. Y.S. and T.A. performed the evolutionary analyses. K.N., T.A., and M.A. wrote the

1196

manuscript.

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Competing interests: The authors declare that they have no competing interests.

1198

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