Crassulacean acid metabolism (CAM) is a specialized mode of photosynthesis that offers the potential to engineer improved water‐use efficiency (WUE) and drought resilience in C3plants while sustaining productivity in the hotter and drier climates that are predicted for much of the world. CAM species show an inverted pattern of stomatal opening and closing across the diel cycle, which conserves water and provides a means of maintaining growth in hot, water‐limited environments. Recent genome sequencing of the constitutive model CAM species
In the leaf epidermis, stomatal pores allow gas exchange between plants and the environment. The production of stomatal guard cells requires the lineage cells to divide asymmetrically. In this Insight review, we describe an emerging picture of how intrinsic molecules drive stomatal asymmetric cell division in multidimensions, from transcriptional activities in the nucleus to the dynamic assembly of the polarity complex at the cell cortex. Given the significant roles of stomatal activity in plant responses to environmental changes, we incorporate recent advances in external cues feeding into the regulation of core molecular machinery required for stomatal development. The work we discuss here is mainly based on the dicot plant
- NSF-PAR ID:
- 10447575
- Publisher / Repository:
- Wiley-Blackwell
- Date Published:
- Journal Name:
- New Phytologist
- Volume:
- 232
- Issue:
- 1
- ISSN:
- 0028-646X
- Page Range / eLocation ID:
- p. 60-67
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
more » « less
Summary Kalanchoë fedtschenkoi provides a platform for elucidating the ensemble of proteins that link photosynthetic metabolism with stomatal movement, and that protect CAM plants from harsh environmental conditions. We describe a large‐scale proteomics analysis to characterize and compare proteins, as well as diel changes in their abundance in guard cell‐enriched epidermis and mesophyll cells from leaves ofK. fedtschenkoi . Proteins implicated in processes that encompass respiration, the transport of water and CO2, stomatal regulation, and CAM biochemistry are highlighted and discussed. Diel rescheduling of guard cell starch turnover inK. fedtschenkoi compared with that observed in Arabidopsis is reported and tissue‐specific localization in the epidermis and mesophyll of isozymes implicated in starch and malate turnover are discussed in line with the contrasting roles for these metabolites within the CAM mesophyll and stomatal complex. These data reveal the proteins and the biological processes enriched in each layer and provide key information for studies aiming to adapt plants to hot and dry environments by modifying leaf physiology for improved plant sustainability. -
more » « less
Summary Protein phosphorylation is a major molecular switch involved in the regulation of stomatal opening and closure. Previous research defined interaction between MAP kinase 12 and Raf‐like kinase HT1 as a required step for stomatal movements caused by changes in CO2concentration. However, whether MPK12 kinase activity is required for regulation of CO2‐induced stomatal responses warrants in‐depth investigation.
We apply genetic, biochemical, and structural modeling approaches to examining the noncatalytic role of MPK12 in guard cell CO2signaling that relies on allosteric inhibition of HT1.
We show that CO2/HCO3−‐enhanced MPK12 interaction with HT1 is independent of its kinase activity. By analyzing gas exchange of plant lines expressing various kinase‐dead and constitutively active versions of MPK12 in a plant line where
MPK12 is deleted, we confirmed that CO2‐dependent stomatal responses rely on MPK12's ability to bind to HT1, but not its kinase activity. We also demonstrate that purified MPK12 and HT1 proteins form a heterodimer in the presence of CO2/HCO3−and present structural modeling that explains the MPK12:HT1 interaction interface.These data add to the model that MPK12 kinase‐activity‐independent interaction with HT1 functions as a molecular switch by which guard cells sense changes in atmospheric CO2concentration.
-
more » « less
<bold>Summary</bold> Cytosolic calcium concentration ([Ca2+]cyt) and heterotrimeric G‐proteins are universal eukaryotic signaling elements. In plant guard cells, extracellular calcium (Cao) is as strong a stimulus for stomatal closure as the phytohormone abscisic acid (
ABA ), but underlying mechanisms remain elusive. Here, we report that the sole Arabidopsis heterotrimeric Gβ subunit,AGB 1, is required for four guard cell Caoresponses: induction of stomatal closure; inhibition of stomatal opening; [Ca2+]cytoscillation; and inositol 1,4,5‐trisphosphate (InsP3) production. Stomata in wild‐type Arabidopsis (Col) and in mutants of the canonical Gα subunit,GPA 1agb1 mutants andagb1 /gpa1 double‐mutants, as well as those of theagg1agg2 Gγ double‐mutant, were insensitive to Cao. These behaviors contrast withABA ‐regulated stomatal movements, which involveGPA 1 andAGB 1/AGG 3 dimers, illustrating differential partitioning of G‐protein subunits among stimuli with similar ultimate impacts, which may facilitate stimulus‐specific encoding.AGB 1NO production, but lostYC 3.6‐detected [Ca2+]cytoscillations in response to Cao, initiating only a single [Ca2+]cytspike. Experimentally imposed [Ca2+]cytoscillations restored stomatal closure inagb1 . Yeast two‐hybrid and bimolecular complementation fluorescence experiments revealed thatAGB 1 interacts with phospholipase Cs (PLCs), and Caoinduced InsP3 production in Col but not inagb1 . In sum, G‐protein signaling viaAGB 1/AGG 1/AGG 2 is essential for Cao‐regulation of stomatal apertures, and stomatal movements in response to Caoapparently require Ca2+‐induced Ca2+release that is likely dependent on Gβγ interaction withPLC s leading to InsP3 production. -
more » « less
Stomatal pore apertures are narrowing globally due to the continuing rise in atmospheric [CO2]. CO2elevation and the plant hormone abscisic acid (ABA) both induce rapid stomatal closure. However, the underlying signal transduction mechanisms for CO2/ABA interaction remain unclear. Two models have been considered: (
i ) CO2elevation enhances ABA concentrations and/or early ABA signaling in guard cells to induce stomatal closure and (ii ) CO2signaling merges with ABA at OST1/SnRK2.6 protein kinase activation. Here we use genetics, ABA-reporter imaging, stomatal conductance, patch clamp, and biochemical analyses to investigate these models. The strong ABA biosynthesis mutantsnced3/nced5 andaba2-1 remain responsive to CO2elevation. Rapid CO2-triggered stomatal closure in PYR/RCAR ABA receptor quadruple and hextuple mutants is not disrupted but delayed. Time-resolved ABA concentration monitoring in guard cells using a FRET-based ABA-reporter, ABAleon2.15, and ABA reporter gene assays suggest that CO2elevation does not trigger [ABA] increases in guard cells, in contrast to control ABA exposures. Moreover, CO2activates guard cell S-type anion channels innced3/nced5 and ABA receptor hextuple mutants. Unexpectedly, in-gel protein kinase assays show that unlike ABA, elevated CO2does not activate OST1/SnRK2 kinases in guard cells. The present study points to a model in which rapid CO2signal transduction leading to stomatal closure occurs via an ABA-independent pathway downstream of OST1/SnRK2.6. Basal ABA signaling and OST1/SnRK2 activity are required to facilitate the stomatal response to elevated CO2. These findings provide insights into the interaction between CO2/ABA signal transduction in light of the continuing rise in atmospheric [CO2]. -
more » « less
Abstract Stomatal opening in the light, observed in nearly all vascular land plants, is essential for providing access to atmospheric CO2 for photosynthesis. The speed of stomatal opening in the light is critical for maximizing carbon gain in environments in which light intensity changes, yet we have little understanding of how other environmental signals, particularly evaporative demand driven by vapor pressure deficit (VPD) influences the kinetics of this response. In angiosperms, and some fern species from the family Marsileaceae, a mechanical interaction between the guard cells and the epidermal cells determines the aperture of the pore. Here, we examine whether this mechanical interaction influences the speed of stomatal opening in the light. To test this, we investigated the speed of stomatal opening in response to light across a range of VPDs in seven plant species spanning the evolutionary diversity of guard cell and epidermal cell mechanical interactions. We found that stomatal opening speed is a function of evaporative demand in angiosperm species and Marsilea, which have guard cell and epidermal cell mechanical interactions. Stomatal opening speeds did not change across a range of VPD in species of gymnosperm and fern, which do not have guard cell mechanical interactions with the epidermis. We find that guard cell and epidermal cell mechanical interactions may play a key role in regulating stomatal responsiveness to light. These results provide valuable insight into the adaptive relevance of mechanical advantage.
