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Rare sugar d-allose suppresses gibberellin signaling through hexokinase-dependent pathway in Oryza sativa L.

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Abstract

One of the rare sugars, d-allose, which is the epimer of d-glucose at C3, has an inhibitory effect on rice growth, but the molecular mechanisms of the growth inhibition by d-allose were unknown. The growth inhibition caused by d-allose was prevented by treatment with hexokinase inhibitors, d-mannoheptulose and N-acetyl-d-glucosamine. Furthermore, the Arabidopsis glucose-insensitive2 (gin2) mutant, which is a loss-of-function mutant of the glucose sensor AtHXK1, showed a d-allose-insensitive phenotype. d-Allose strongly inhibited the gibberellin-dependent responses such as elongation of the second leaf sheath and induction of α-amylase in embryo-less half rice seeds. The growth of the slender rice1 (slr1) mutant, which exhibits a constitutive gibberellin-responsive phenotype, was also inhibited by d-allose, and the growth inhibition of the slr1 mutant by d-allose was also prevented by d-mannoheptulose treatment. The expressions of gibberellin-responsive genes were down-regulated by d-allose treatment, and the down-regulations of gibberellin-responsive genes were also prevented by d-mannoheptulose treatment. These findings reveal that d-allose inhibits the gibberellin-signaling through a hexokinase-dependent pathway.

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Abbreviations

GA:

Gibberellin

gin2 :

Glucose-insensitive2

GlcNAc:

N-acetyl-d-glucosamine

HXK:

Hexokinase

MNH:

d-Mannoheptulose

slr1 :

Slender rice1

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Acknowledgments

We gratefully thank Dr. Makoto Matsuoka, Nagoya University, for gifting of the seeds of rice slr 1 mutant. This study was supported by the Program for Promotion of Basic Research Activities for Innovative Biosciences (PROBRAIN).

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Authors and Affiliations

  1. Faculty of Agriculture, Rare Sugar Research Center and Gene Research Center, Kagawa University, Miki, Kagawa, 761-0795, Japan

    Takeshi Fukumoto, Akihito Kano, Kouhei Ohtani, Yumiko Yamasaki-Kokudo, Bong-Gyu Kim, Kouji Hosotani, Miu Saito, Chikage Shirakawa, Shigeyuki Tajima, Ken Izumori, Yasuomi Tada, Kazuya Ichimura, Kenji Gomi & Kazuya Akimitsu

  2. Mitsui Chemicals Agro Co. Ltd, Yasu, Shiga, 520-2342, Japan

    Toshiaki Ohara, Yoshio Shigematsu & Keiji Tanaka

  3. Shikoku Research Institute Inc., Yashima-nishi, Takamatsu, 761-0192, Japan

    Yutaka Ishida

  4. National Institute of Agrobiological Sciences, Tsukuba, 305-8602, Japan

    Yoko Nishizawa

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  1. Takeshi Fukumoto
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  2. Akihito Kano
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Correspondence to Kazuya Akimitsu.

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425_2011_1463_MOESM1_ESM.tif

Fig. S1 (Supplement 1) Schematic concept of Izumo-ring for bioproduction of rare sugars. The hexose Izumo-ring allows the bioproduction of all hexose sugars using enzymatic reactions of d-tagatose 3-epimerase, polyol dehydrogenases, and aldose isomerases (Izumori 2002, 2006; Figure was taken from Izumori 2006) (TIFF 6066 kb)

Fig. S2 (Supplement 2) A scheme model to explain the mode of actions of d-allose to inhibit rice growth (TIFF 489 kb)

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Fukumoto, T., Kano, A., Ohtani, K. et al. Rare sugar d-allose suppresses gibberellin signaling through hexokinase-dependent pathway in Oryza sativa L.. Planta 234, 1083–1095 (2011). https://doi.org/10.1007/s00425-011-1463-3

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