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<p>Anaerobic germination enables rice (<i>Oryza sativa</i> L.) to establish seedlings under flooding by elongating the coleoptile through starch mobilization. Although heterotrimeric G proteins regulate plant growth and stress responses, their role in anaerobic germination is unclear. Here, we show that the rice Gγ subunit <i>RGG3</i>/<i>GS3</i>, particularly its cysteine-rich C-terminal domain, is indispensable for coleoptile elongation under oxygen deficiency. In contrast to their divergent developmental phenotypes in grain length and plant stature, both <i>rgg3</i> null mutants and C-terminal deletion lines (<i>RGG3-ΔCys</i>) exhibited a shared defect: impaired coleoptile elongation during anaerobic germination. This was associated with reduced starch degradation and decreased expression of multiple α-amylase (<i>AMY</i>) genes. Transcript profiling indicates that <i>RGG3</i> promotes two <i>AMY</i>-activating modules—the sugar-starvation–responsive CIPK15–SnRK1A–MYBS1 cascade and the hormone-regulated GAMYB–DOF3 pathway—and integrates their outputs at <i>AMY</i> promoters bearing conserved TA and pyrimidine boxes. Consistent with the activation of the CIPK15–SnRK1A–MYBS1 module, <i>RGG3</i> increased the expression of trehalose-6-phosphate (Tre6P) phosphatases (<i>TPP1</i>/<i>TPP7</i>), which would lower Tre6P levels. Because Tre6P is an inhibitor of SnRK1A, reduced Tre6P would relieve this inhibition and favor SnRK1A activation. Together, these results position <i>RGG3</i> as a hub that coordinates metabolic (CIPK15–SnRK1A–MYBS1) and hormonal (GAMYB–DOF3) signaling to couple starch mobilization with coleoptile elongation during anaerobic germination, revealing an uncharacterized role for G-protein signaling in flooding tolerance and suggesting a target for improving direct-seeded rice.</p>

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The heterotrimeric G protein γ3 subunit, RGG3/GS3, integrates sugar-starvation and hormone-responsive signaling pathways to promote coleoptile elongation during anaerobic germination in rice

  • 期刊论文

  • 发表日期：

    2025年12月23日

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  • Taichi Takashima,
  • Hikaru Azumahara,
  • Haru Hirano,
  • Soshi Hirata,
  • Mika Fukuda,
  • Sagar Lamsal,
  • Kotaro Miura,
  • Yukimoto Iwasaki,
  • Takeshi Fukao

摘要

Anaerobic germination enables rice (Oryza sativa L.) to establish seedlings under flooding by elongating the coleoptile through starch mobilization. Although heterotrimeric G proteins regulate plant growth and stress responses, their role in anaerobic germination is unclear. Here, we show that the rice Gγ subunit RGG3/GS3, particularly its cysteine-rich C-terminal domain, is indispensable for coleoptile elongation under oxygen deficiency. In contrast to their divergent developmental phenotypes in grain length and plant stature, both rgg3 null mutants and C-terminal deletion lines (RGG3-ΔCys) exhibited a shared defect: impaired coleoptile elongation during anaerobic germination. This was associated with reduced starch degradation and decreased expression of multiple α-amylase (AMY) genes. Transcript profiling indicates that RGG3 promotes two AMY-activating modules—the sugar-starvation–responsive CIPK15–SnRK1A–MYBS1 cascade and the hormone-regulated GAMYB–DOF3 pathway—and integrates their outputs at AMY promoters bearing conserved TA and pyrimidine boxes. Consistent with the activation of the CIPK15–SnRK1A–MYBS1 module, RGG3 increased the expression of trehalose-6-phosphate (Tre6P) phosphatases (TPP1/TPP7), which would lower Tre6P levels. Because Tre6P is an inhibitor of SnRK1A, reduced Tre6P would relieve this inhibition and favor SnRK1A activation. Together, these results position RGG3 as a hub that coordinates metabolic (CIPK15–SnRK1A–MYBS1) and hormonal (GAMYB–DOF3) signaling to couple starch mobilization with coleoptile elongation during anaerobic germination, revealing an uncharacterized role for G-protein signaling in flooding tolerance and suggesting a target for improving direct-seeded rice.