Global climate change-caused drought stress, high temperatures and other extreme weather profoundly impact plant growth and development, restricting sustainable crop production. To cope with various environmental stimuli, plants can optimize the opening and closing of stomata to balance CO2 uptake for photosynthesis and water loss from leaves. Guard cells perceive and integrate various signals to adjust stomatal pores through turgor pressure regulation. Molecular mechanisms and signaling networks underlying the stomatal movements in response to environmental stresses have been extensively studied and elucidated. This review focuses on the molecular mechanisms of stomatal movements mediated by abscisic acid, light, CO2 , reactive oxygen species, pathogens, temperature, and other phytohormones. We discussed the significance of elucidating the integrative mechanisms that regulate stomatal movements in helping design smart crops with enhanced water use efficiency and resilience in a climate-changing world.

Integrative regulatory mechanisms of stomatal movements under changing climate.

Stomata are tiny pores on leaf surfaces essential for plant transpiration and photosynthesis. As the connecting hub between the atmosphere, plants and soil, stomata play a significant role in global carbon and water cycles. The shape and function of stomata are physically constrained by stomatal walls. Compared to the extensively studied genetic mechanisms of stomatal development and guard cell signaling, recent progress is only beginning to uncover the role of plant cell walls in stomatal development and dynamics. In this review, we summarize the research on cell walls of the kidney-shaped stomata from dicots and the dumbbell-shaped stomata from grasses. As the dynamic response of grass stomata is closely linked to its anatomical features that are limited by cell walls, we discuss the potential of plant cell walls as crucial targets for crop engineering to enhance carbon assimilation and water use efficiency. 

Plant Cell Walls: Emerging Targets of Stomata Engineering to Improve Photosynthesis and Water Use Efficiency

Global climate change is affecting plant photosynthesis and transpiration processes, as well as increasing weather extremes impacting socio-political and environmental events and decisions for decades to come. One major research challenge in plant biology and ecology is the interaction of photosynthesis with the environment. Stomata control plant gas exchange and their evolution was a crucial innovation that facilitated the earliest land plants to colonize terrestrial environments. Stomata couple homoiohydry, together with cuticles, intercellular gas space, with the endohydric water-conducting system, enabling plants to adapt and diversify across the planet. Plants control stomatal movement in response to environmental change through regulating guard cell turgor mediated by membrane transporters and signaling transduction. However, the origin, evolution, and active control of stomata remain controversial topics. We first review stomatal evolution and diversity, providing fossil and phylogenetic evidence of their origins. We summarize functional evolution of guard cell membrane transporters in the context of climate changes and environmental stresses. Our analyses show that the core signaling elements of stomatal movement are more ancient than stomata, while genes involved in stomatal development co-evolved de novo with the earliest stomata. These results suggest that novel stomatal development-specific genes were acquired during plant evolution, whereas genes regulating stomatal movement, especially cell signaling pathways, were inherited ancestrally and co-opted by dynamic functional differentiation. These two processes reflect the different adaptation strategies during land plant evolution.

Stomatal evolution and plant adaptation to future climate.

Stomata serve as the battleground between plants and plant pathogens. Plants can perceive pathogens, inducing closure of the stomatal pore, while pathogens can overcome this immune response with their phytotoxins and elicitors. In this review, we summarize new discoveries in stomata–pathogen interactions. Recent studies have shown that stomatal movement continues to occur in a close-open-close-open pattern during bacterium infection, bringing a new understanding of stomatal immunity. Furthermore, the canonical pattern-triggered immunity pathway and ion channel activities seem to be common to plant–pathogen interactions outside of the well-studied Arabidopsis – Pseudomonas pathosystem. These developments can be useful to aid in the goal of crop improvement. New technologies to study intact leaves and advances in available omics data sets provide new methods for understanding the fight at the stomatal gate. Future studies should aim to further investigate the defense–growth trade-off in relation to stomatal immunity, as little is known at this time. 

Fighting for Survival at the Stomatal Gate

Overexpression of cassava melatonin receptor PMTR1 plays dual roles in development under light and dark conditions in Arabidopsis

Aluminum (Al) stress triggers the accumulation of hydrogen peroxide (H2O2) in roots. However, whether H2O2 plays a regulatory role in aluminum resistance remains unclear. In this study, we show that H2O2 plays a crucial role in regulation of Al resistance, which is modulated by the mitochondrion-localized pentatricopeptide repeat protein REGULATION OF ALMT1 EXPRESSION 6 (RAE6). Mutation in RAE6 impairs the activity of complex I of the mitochondrial electron transport chain, resulting in the accumulation of H2O2 and increased sensitivity to Al. Our results suggest that higher H2O2 concentrations promote the oxidation of SENSITIVE TO PROTON RHIZOTOXICITY 1 (STOP1), an essential transcription factor that promotes Al resistance, thereby promoting its degradation by enhancing the interaction between STOP1 and the F-box protein RAE1. Conversely, decreasing H2O2 levels or blocking the oxidation of STOP1 leads to greater STOP1 stability and increased Al resistance. Moreover, we show that the thioredoxin TRX1 interacts with STOP1 to catalyze its chemical reduction. Thus, our results highlight the importance of H2O2 in Al resistance and regulation of STOP1 stability in Arabidopsis (Arabidopsis thaliana).

H2O2 negatively regulates aluminum resistance via oxidation and degradation of the transcription factor STOP1.

Multicellular organisms such as plants contain various cell types with specialized functions. Analyzing the characteristics of each cell type reveals specific cell functions and enhances our understanding of organization and function at the organismal level. Guard cells (GC) are specialized epidermal cells that regulate the movement of the stomata and gaseous exchange, and provide a model genetic system for analyzing cell fate, signaling and function. Several proteomics analyses of GC are available, but these are limited in depth. Here we used enzymatic isolation and flow cytometry to enrich for GC and mesophyll cell protoplasts and perform in-depth proteomics in these two major cell types in Arabidopsis leaves. We identified ~3,000 proteins not previously found in the GC proteome and more than 600 proteins that may be specific to GC. The depth of our proteomics enabled us to uncover a guard cell-specific kinase cascade whereby Raf15 and Snf1-related kinase2.6 (SnRK2.6)/OST1(open stomata 1) mediate abscisic acid (ABA)-induced stomatal closure. RAF15 directly phosphorylated SnRK2.6/OST1 at the conserved Ser175 residue in its activation loop and was sufficient to reactivate the inactive form of SnRK2.6/OST1. ABA-triggered SnRK2.6/OST1 activation and stomatal closure was impaired in raf15 mutants. We also showed enrichment of enzymes and flavone metabolism in GC, and consistent, dramatic accumulation of flavone metabolites. Our study answers the long-standing question of how ABA activates SnRK2.6/OST1 in guard cells and represents a resource potentially providing further insights into the molecular basis of GC and mesophyll cell development, metabolism, structure, and function. This article is protected by copyright. All rights reserved.

https://onlinelibrary.wiley.com/doi/pdfdirect/10.1111/jipb.13536

Cell type-specific proteomics uncovers a RAF15-SnRK2.6/OST1 kinase cascade in guard cells.

Redox homeostasis and Fe-S protein maturation are critical for chloroplast function. Chloroplast-localized glutaredoxins (Grxs) are versatile enzymes that function either as oxidoreductases or Fe-S cluster transferases. However, their target proteins and underlying molecular mechanisms remain incompletely understood. Here, we demonstrate that the cysteine 34 within the active site motif of chloroplast-localized Arabidopsis GrxS12 is the key residue governing its oxidoreductase activity, while the C-terminal cysteine 92 plays a secondary role. These cysteines undergo glutathionylation or form an intramolecular disulfide bond, which can be reduced by Trx-m1. Although GrxS12 is unable to bind Fe-S clusters itself, it interacts with and reduces the Fe-S cluster assembly protein SufB, thereby regulating Fe-S protein maturation. Loss of GrxS12 induces redox alterations of multiple chloroplast proteins, increased oxidation of SufB, and decreased abundances of several Fe-S proteins. These changes likely underlie the observed structural damage to chloroplasts, reduced photosynthetic efficiency, and slower growth in grxs12 mutants. Our results reveal a novel mechanism by which GrxS12 regulates chloroplast Fe-S cluster biogenesis through its oxidoreductase activity.

Chloroplast glutaredoxin S12 regulates photosynthesis and growth through redox modulation of SufB.

Cyclin-dependent kinase 1 (CDK1) is the pivotal kinase responsible for initiating cell division. Its activation is dependent on binding to regulatory cyclins, such as CCNB1. Our research demonstrates that copper binding to both CDK1 and CCNB1 is essential for activating CDK1 in cells. Mutations in the copper-binding amino acids of either CDK1 or CCNB1 do not disrupt their interaction but are unable to activate CDK1. We also reveal that CCNB1 facilitates the transfer of copper from ATOX1 to CDK1, consequently activating its kinase function. Disruption of copper transfer through the ATOX1-CCNB1-CDK1 pathway can impede CDK1 activation and halt cell cycle progression. In summary, our findings elucidate a mechanism through which copper promotes CDK1 activation and the G2/M transition in the cell cycle. These results could provide insight into the acquisition of proliferative properties associated with increased copper levels in cancer and offer targets for cancer therapy. Intracellular copper concentration has been linked to cell proliferation. Here, the authors demonstrate that copper binding to both Cyclin-dependent kinase 1 (CDK1) and CCNB1 is essential for activating CDK1 and promoting the G2/M transition in the cell cycle.

Copper is essential for cyclin B1-mediated CDK1 activation

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H2O2 negatively regulates aluminum resistance via oxidation and degradation of the transcription factor STOP1.

Cell type-specific proteomics uncovers a RAF15-SnRK2.6/OST1 kinase cascade in guard cells.

Chloroplast glutaredoxin S12 regulates photosynthesis and growth through redox modulation of SufB.

Copper is essential for cyclin B1-mediated CDK1 activation