Hydrogen peroxide is required for light-induced stomatal opening across different plant species.

Stomatal movement is vital for plants to exchange gases and adaption to terrestrial habitats, which is regulated by environmental and phytohormonal signals. Here, we demonstrate that hydrogen peroxide (H2O2) is required for light-induced stomatal opening. H2O2 accumulates specifically in guard cells even when plants are under unstressed conditions. Reducing H2O2 content through chemical treatments or genetic manipulations results in impaired stomatal opening in response to light. This phenomenon is observed across different plant species, including lycopodium, fern, and monocotyledonous wheat. Additionally, we show that H2O2 induces the nuclear localization of KIN10 protein, the catalytic subunit of plant energy sensor SnRK1. The nuclear-localized KIN10 interacts with and phosphorylates the bZIP transcription factor bZIP30, leading to the formation of a heterodimer between bZIP30 and BRASSINAZOLE-RESISTANT1 (BZR1), the master regulator of brassinosteroid signaling. This heterodimer complex activates the expression of amylase, which enables guard cell starch degradation and promotes stomatal opening. Overall, these findings suggest that H2O2 plays a critical role in light-induced stomatal opening across different plant species.

Brassinosteroid signaling and molecular crosstalk with nutrients in plants.

As sessile organisms, plants have evolved sophisticated mechanisms to optimize their growth and development in response to fluctuating nutrient levels. Brassinosteroids (BRs) are a group of plant steroid hormones that play critical roles in plant growth and developmental processes as well as plant responses to environmental stimuli. Recently, multiple molecular mechanisms have been proposed to explain the integration of BRs with different nutrient signaling processes to coordinate gene expression, metabolism, growth, and survival. Here, we review recent advances in understanding the molecular regulatory mechanisms of the BR signaling pathway and the multifaceted roles of BR in the intertwined sensing, signaling, and metabolic processes of sugar, nitrogen, phosphorus, and iron. Further understanding and exploring these BR-related processes and mechanisms will facilitate advances in crop breeding for higher resource efficiency.

Regulatory functions of cellular energy sensor SnRK1 for nitrate signalling through NLP7 repression.

The coordinated metabolism of carbon and nitrogen is essential for optimal plant growth and development. Nitrate is an important molecular signal for plant adaptation to a changing environment, but how nitrate regulates plant growth under carbon deficiency conditions remains unclear. Here we show that the evolutionarily conserved energy sensor SnRK1 negatively regulates the nitrate signalling pathway. Nitrate promoted plant growth and downstream gene expression, but such effects were repressed when plants were grown under carbon deficiency conditions. Mutation of KIN10, the α-catalytic subunit of SnRK1, partially suppressed the inhibitory effects of carbon deficiency on nitrate-mediated plant growth. KIN10 phosphorylated NLP7, the master regulator of the nitrate signalling pathway, to promote its cytoplasmic localization and degradation. Furthermore, nitrate depletion induced KIN10 accumulation, whereas nitrate treatment promoted KIN10 degradation. Such KIN10-mediated NLP7 regulation allows carbon and nitrate availability to control optimal nitrate signalling and ensures the coordination of carbon and nitrogen metabolism in plants.

Spatially patterned hydrogen peroxide orchestrates stomatal development in Arabidopsis.

Stomatal pores allow gas exchange between plant and atmosphere. Stomatal development is regulated by multiple intrinsic developmental and environmental signals. Here, we show that spatially patterned hydrogen peroxide (H2O2) plays an essential role in stomatal development. H2O2 is remarkably enriched in meristemoids, which is established by spatial expression patterns of H2O2-scavenging enzyme CAT2 and APX1. SPEECHLESS (SPCH), a master regulator of stomatal development, directly binds to the promoters of CAT2 and APX1 to repress their expression in meristemoid cells. Mutations in CAT2 or APX1 result in an increased stomatal index. Ectopic expression of CAT2 driven by SPCH promoter significantly inhibits the stomatal development. Furthermore, H2O2 activates the energy sensor SnRK1 by inducing the nuclear localization of the catalytic α-subunit KIN10, which stabilizes SPCH to promote stomatal development. Overall, these results demonstrate that the spatial pattern of H2O2 in epidermal leaves is critical for the optimal stomatal development in Arabidopsis.

TOR and SnRK1 fine tune SPEECHLESS transcription and protein stability to optimize stomatal development in response to exogenously supplied sugar.

In Arabidopsis, the differentiation of epidermal cells into stomata is regulated by endogenous and environmental signals. Sugar is required for plant epidermal cell proliferation and differentiation. However, it is unclear how epidermal cells maintain division and differentiation to generate proper amounts of stomata in response to different sugar availability. Here, we show that two evolutionarily conserved kinase Snf1-related protein kinase 1 (SnRK1) and Target of rapamycin (TOR) play critical roles in the regulation of stomatal development under different sugar availability. When plants are grown on a medium containing 1% sucrose, sucrose-activated TOR promotes the stomatal development by inducing the expression of SPEECHLESS (SPCH), a master regulator of stomatal development. SnRK1 promotes stomatal development through phosphorylating and stabilizing SPCH. However, under the high sucrose conditions, the highly accumulated trehalose-6-phosphate (Tre6P) represses the activity of KIN10, the catalytic α-subunit of SnRK1, by reducing the interaction between KIN10 and its upstream kinase, consequently promoting SPCH degradation and inhibiting stomatal development. Our findings revealed that TOR and SnRK1 finely regulate SPCH expression and protein stability to optimize the stomatal development in response to exogenously supplied sugar.

TOR promotes guard cell starch degradation by regulating the activity of ß-AMYLASE1 in Arabidopsis.

Starch is the main energy storage carbohydrate in plants and serves as an essential carbon storage molecule for plant metabolism and growth under changing environmental conditions. The TARGET of RAPAMYCIN (TOR) kinase is an evolutionarily conserved master regulator that integrates energy, nutrient, hormone, and stress signaling to regulate growth in all eukaryotes. Here, we demonstrate that TOR promotes guard cell starch degradation and induces stomatal opening in Arabidopsis thaliana. Starvation caused by plants growing under short photoperiod or low light photon irradiance, as well as inactivation of TOR, impaired guard cell starch degradation and stomatal opening. Sugar and TOR induce the accumulation of ß-AMYLASE1 (BAM1), which is responsible for starch degradation in guard cells. The plant steroid hormone brassinosteroid and transcription factor BRASSINAZOLE-RESISTANT1 play crucial roles in sugar-promoted expression of BAM1. Furthermore, sugar supply induced BAM1 accumulation, but TOR inactivation led to BAM1 degradation, and the effects of TOR inactivation on BAM1 degradation were abolished by the inhibition of autophagy and proteasome pathways or by phospho-mimicking mutation of BAM1 at serine-31. Such regulation of BAM1 activity by sugar-TOR signaling allows carbon availability to regulate guard cell starch metabolism and stomatal movement, ensuring optimal photosynthesis efficiency of plants.