Sugar status in pre-existing leaves determines systemic stomatal development within newly developing leaves

Qin-Xin Bao, Xin Rong Mu, Chen Tong, Cong Li, Wen Zhe Tao, Sheng Ting Zhao, Xin Yue Liu, Wan Ni Wang, Yun Ting Wei, Fu Huan Yu, Jing wen Wang, Zhi Lan Sun, Bing Ling Fan, Jia Sun, Chen Wang, Gary J. Loake, Lai-Sheng Meng

Research output: Contribution to journalArticlepeer-review

Abstract / Description of output

Stomata are pores found in the epidermis of stems or leaves, that modulates both plant gas exchange and water/nutrient uptake. The development and function of plant stomata is regulated by a diverse range of environmental cues. However, how carbohydrate status in pre-existing leaves determines systemic stomatal formation within newly developing leaves has remained obscure. The glucose (Glc) sensor HEXOKINASE1 (HXK1) has been reported to decrease the stability of an ethylene/Glc signaling transcriptional regulator, EIN3 (ETHYLENE INSENSITIVE3). EIN3 in turn directly represses the expression of SUC2 (SUCROSE TRANSPORTER 2), encoding a master transporter of sucrose (Suc). Further, KIN10, a nuclear regulator involved in energy homeostasis, has been reported to repress the transcription factor SPCH (SPEECHLESS), a master regulator of stomatal development, to orchestrate stomatal development. Here, we demonstrate that the Glc status of pre-existing leaves determines systemic stomatal development within newly developing leaves by the HXK1—¦EIN3—¦SUC2 module. Further, increasing Glc levels in pre-existing leaves results in a HXK1-dependent decrease of EIN3 and increase of SUC2, triggering the perception, amplification and relay of HXK1-dependent Glc signaling and thereby triggering Suc transport from mature to newly developing leaves. The HXK1—¦EIN3—¦SUC2 molecular module thereby drives systemic Suc transport from pre-existing leaves to newly developing leaves. Subsequently, increasing Suc levels within newly developing leaves promotes stomatal formation through the known KIN10⟶ SPCH module. Our findings thus establish how a carbohydrate signal in pre-existing leaves is sensed, amplified and relayed to determine the extent of systemic stomatal development within newly developing leaves.
Original languageEnglish
Article numbere2302854120
Number of pages29
JournalProceedings of the National Academy of Sciences (PNAS)
Early online date5 Jun 2023
DOIs
Publication statusPublished - 5 Jun 2023

Keywords / Materials (for Non-textual outputs)

  • ethylene-insensitive3 (EIN3)
  • sucrose (Suc)
  • sucrose transporter 2 (SUC2)
  • stomatal development
  • sucrose phloem transport

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