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

Abstract Background Whole genome duplication (polyploidization) is a dominant force in sympatric speciation, particularly in plants. Genome doubling instantly poses a barrier to gene flow owing to the strong crossing incompatibilities between individuals differing in ploidy. The strength of the barrier, however, varies from species to species and recent genetic investigations revealed cases of rampant interploidy introgression in multiple ploidy-variable species. Scope Here, we review novel insights into the frequency of interploidy gene flow in natural systems and summarize the underlying mechanisms promoting interploidy gene flow. Field surveys, occasionally complemented by crossing experiments, suggest frequent opportunities for interploidy gene flow, particularly in the direction from diploid to tetraploid, and between (higher) polyploids. However, a scarcity of accompanying population genetic evidence and a virtual lack of integration of these approaches leave the underlying mechanisms and levels of realized interploidy gene flow in nature largely unknown. Finally, we discuss potential consequences of interploidy genome permeability on polyploid speciation and adaptation and highlight novel avenues that have just recently been opened by the very first genomic studies of ploidy-variable species. Standing in stark contrast with rapidly accumulating evidence for evolutionary importance of homoploid introgression, similar cases in ploidy-variable systems are yet to be documented. Conclusions The genomics era provides novel opportunity to re-evaluate the role of interploidy introgression in speciation and adaptation. To achieve this goal, interdisciplinary studies bordering ecology and population genetics and genomics are needed. 

Ploidy as a leaky reproductive barrier: mechanisms, rates and evolutionary significance of interploidy gene flow

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.

Understanding how species diversify is a long-standing question in biology. The allopatric speciation model is a classic hypothesis to explain the speciation process. This model supposes that there is no gene flow during the divergence process of geographically isolated populations. On the contrary, the speciation with gene flow model supposes that gene flow does occur during the speciation process. Whether allopatric species have gene flow during the speciation process is still an open question. We used the genetic information from 31 loci of 24 Chinese Bamboo Partridges (Bambusicola thoracicus) and 23 Taiwan Bamboo Partridges (B. sonorivox) to infer the gene flow model of the two species, using the approximate Bayesian computation (ABC) model. The ecological niche model was used to infer the paleo-distribution during the glacial period. We also tested whether the two species had a conserved ecological niche by means of a background similarity test. The genetic data suggested that the post-divergence gene flow between the two species was terminated before the mid-Pleistocene. Furthermore, our ecological niche modeling suggested that their ecological niches were highly conserved, and that they shared an overlapping potential distribution range in the last glacial maximum. The allopatric speciation model cannot explain the speciation process of the two Bamboo Partridges. The results of this study supported a scenario in which speciation with gene flow occurring between the allopatric species and have contributed to our understanding of the speciation process.

/pdf/multilocus-phylogeography-and-ecological-niche-modeling-1hjk7swxmy.pdf

Multilocus phylogeography and ecological niche modeling suggest speciation with gene flow between the two Bamboo Partridges

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

Multilocus phylogeography and ecological niche modeling suggest speciation with gene flow between the two Bamboo Partridges