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In most plants, sucrose, a major storage sugar, is transported into sink organs to support their growth. This key physiological process is dependent on the function of sucrose transporters. Sucrose export from source tissues is predominantly controlled through the activity of SUCROSE TRANSPORTER 2 (SUC2), required for the loading of sucrose into the phloem of Arabidopsis plants. However, how SUC2 activity is controlled to support root growth remains unclear. Glucose is perceived via the function of HEXOKINASE 1 (HXK1), the only known nuclear glucose sensor. HXK1 negatively regulates the stability of ETHYLENE-INSENSITIVE3 (EIN3), a key ethylene/glucose interaction component. Here we show that HXK1 functions upstream of EIN3 in the regulation of root sink growth mediated by glucose signaling. Furthermore, the transcription factor EIN3 directly inhibits SUC2 activity by binding to the SUC2 promoter, regulating glucose signaling linked to root sink growth. We demonstrate that these molecular components form a HXK1-EIN3-SUC2 module integral to the control of root sink growth. Also, we demonstrate that with increasing age, the HXK1-EIN3-SUC2 module promotes sucrose phloem loading in source tissues thereby elevating sucrose levels in sink roots. As a result, glucose signaling mediated-sink root growth is facilitated. Our findings thus establish a direct molecular link between the HXK1-EIN3-SUC2 module, the source-to sink transport of sucrose and root growth.

Summary: CINV1, converting sucrose into glucose and fructose, is a key entry of carbon into cellular metabolism, and HXK1 functions as a pivotal sensor for glucose. Exogenous sugars trigger the Arabidopsis juvenile-to-adult phase transition via a miR156A/SPL module. However, the endogenous factors that regulate this process remain unclear. In this study, we show that sucrose specifically induced the PAP1 transcription factor directly and positively controls CINV1 activity. Furthermore, we identify a glucose feed-forward loop (sucrose-CINV1-glucose-HXK1-miR156-SPL9-PAP1-CINV1-glucose) that controls CINV1 activity to convert sucrose into glucose signaling to dynamically control the juvenile-to-adult phase transition. Moreover, PAP1 directly binds to the SPL9 promoter, activating SPL9 expression and triggering the sucrose-signaling-mediated juvenile-to-adult phase transition. Therefore, a glucose-signaling feed-forward loop and a sucrose-signaling pathway synergistically regulate the Arabidopsis juvenile-to-adult phase transition. Collectively, we identify a molecular link between the major photosynthate sucrose, the entry point of carbon into cellular metabolism, and the plant juvenile-to-adult phase transition.

Stomata are pores found in the epidermis of stems or leaves that modulate both plant gas exchange and water/nutrient uptake. The development and function of plant stomata are regulated by a diverse range of environmental cues. However, how carbohydrate status in preexisting leaves might determine 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. Here, we demonstrate that the Glc status of preexisting leaves determines systemic stomatal development within newly developing leaves by the HXK1--¦EIN3--¦SUC2 module. Further, increasing Glc levels in preexisting 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 preexisting leaves to newly developing leaves. Subsequently, increasing Suc levels within newly developing leaves promotes stomatal formation through the established KIN10→SPCH module. Our findings thus show how a carbohydrate signal in preexisting leaves is sensed, amplified and relayed to determine the extent of systemic stomatal development within newly developing leaves. [ABSTRACT FROM AUTHOR]