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

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.