Stomatal Guard Cells Co-opted an Ancient ABA-Dependent Desiccation Survival System to Regulate Stomatal Closure

Stomatal guard cells play a key role in gas exchange for photosynthesis and in minimizing transpirational water loss from plants by opening and closing the stomatal pore. The bulk of the osmotic content driving stomatal movements depends on ionic fluxes across both the plasma membrane and tonoplast, the metabolism of organic acids, primarily Mal (malate), and its accumulation and loss. Anion channels at the plasma membrane are thought to comprise a major pathway for Mal efflux during stomatal closure, implicating their key role in linking solute flux with metabolism. Nonetheless, little is known of the regulation of anion channel current (ICl) by cytosolic Mal or its immediate metabolite OAA (oxaloacetate). In the present study, we have examined the impact of Mal, OAA and of the monocarboxylic acid anion acetate in guard cells of Vicia faba L. and report that all three organic acids affect ICl, but with markedly different characteristics and sidedness to their activities. Most prominent was a suppression of ICl by OAA within the physiological range of concentrations found in vivo. These findings indicate a capacity for OAA to co-ordinate organic acid metabolism with ICl through the direct effect of organic acid pool size. The findings of the present study also add perspective to in vivo recordings using acetate-based electrolytes.

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Eukaryotic lipid metabolic pathway is essential for functional chloroplasts and CO2 and light responses in Arabidopsis guard cells

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.1810458115 ◽

2018 ◽

Vol 115 (36) ◽

pp. 9038-9043 ◽

Cited By ~ 9

Author(s):

Juntaro Negi ◽

Shintaro Munemasa ◽

Boseok Song ◽

Ryosuke Tadakuma ◽

Mayumi Fujita ◽

...

Keyword(s):

Metabolic Pathway ◽

Guard Cell ◽

Membrane Lipids ◽

Stomatal Closure ◽

Guard Cells ◽

Land Plant ◽

In The Wild ◽

Stomatal Guard Cells ◽

Guard Cell Chloroplasts ◽

And Function

Stomatal guard cells develop unique chloroplasts in land plant species. However, the developmental mechanisms and function of chloroplasts in guard cells remain unclear. In seed plants, chloroplast membrane lipids are synthesized via two pathways: the prokaryotic and eukaryotic pathways. Here we report the central contribution of endoplasmic reticulum (ER)-derived chloroplast lipids, which are synthesized through the eukaryotic lipid metabolic pathway, in the development of functional guard cell chloroplasts. We gained insight into this pathway by isolating and examining an Arabidopsis mutant, gles1 (green less stomata 1), which had achlorophyllous stomatal guard cells and impaired stomatal responses to CO2 and light. The GLES1 gene encodes a small glycine-rich protein, which is a putative regulatory component of the trigalactosyldiacylglycerol (TGD) protein complex that mediates ER-to-chloroplast lipid transport via the eukaryotic pathway. Lipidomic analysis revealed that in the wild type, the prokaryotic pathway is dysfunctional, specifically in guard cells, whereas in gles1 guard cells, the eukaryotic pathway is also abrogated. CO2-induced stomatal closing and activation of guard cell S-type anion channels that drive stomatal closure were disrupted in gles1 guard cells. In conclusion, the eukaryotic lipid pathway plays an essential role in the development of a sensing/signaling machinery for CO2 and light in guard cell chloroplasts.

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ALA-Induced Flavonols Accumulation in Guard Cells Is Involved in Scavenging H2O2 and Inhibiting Stomatal Closure in Arabidopsis Cotyledons

Frontiers in Plant Science ◽

10.3389/fpls.2016.01713 ◽

2016 ◽

Vol 7 ◽

Cited By ~ 3

Author(s):

Yuyan An ◽

Xinxin Feng ◽

Longbo Liu ◽

Lijun Xiong ◽

Liangju Wang

Keyword(s):

Stomatal Closure ◽

Guard Cells

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Arabidopsis NPF4.6 and NPF5.1 Control Leaf Stomatal Aperture by Regulating Abscisic Acid Transport

Genes ◽

10.3390/genes12060885 ◽

2021 ◽

Vol 12 (6) ◽

pp. 885

Author(s):

Takafumi Shimizu ◽

Yuri Kanno ◽

Hiromi Suzuki ◽

Shunsuke Watanabe ◽

Mitsunori Seo

Keyword(s):

Abscisic Acid ◽

Plant Hormone ◽

Leaf Surface ◽

Stomatal Closure ◽

Guard Cells ◽

Cell Types ◽

Acid Transport ◽

Wild Type ◽

Vascular Tissues ◽

Abscisic Acid Transport

The plant hormone abscisic acid (ABA) is actively synthesized in vascular tissues and transported to guard cells to promote stomatal closure. Although several transmembrane ABA transporters have been identified, how the movement of ABA within plants is regulated is not fully understood. In this study, we determined that Arabidopsis NPF4.6, previously identified as an ABA transporter expressed in vascular tissues, is also present in guard cells and positively regulates stomatal closure in leaves. We also found that mutants defective in NPF5.1 had a higher leaf surface temperature compared to the wild type. Additionally, NPF5.1 mediated cellular ABA uptake when expressed in a heterologous yeast system. Promoter activities of NPF5.1 were detected in several leaf cell types. Taken together, these observations indicate that NPF5.1 negatively regulates stomatal closure by regulating the amount of ABA that can be transported from vascular tissues to guard cells.

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Modulation of frequency and height of cytosolic calcium spikes by plasma membrane anion channels in guard cells

Bioscience Biotechnology and Biochemistry ◽

10.1093/bbb/zbab118 ◽

2021 ◽

Author(s):

Md Tahjib-Ul-Arif ◽

Shintaro Munemasa ◽

Toshiyuki Nakamura ◽

Yoshimasa Nakamura ◽

Yoshiyuki Murata

Keyword(s):

Plasma Membrane ◽

Stomatal Closure ◽

Anion Channel ◽

Guard Cells ◽

Cytosolic Calcium ◽

Peak Height ◽

Extracellular Calcium ◽

Wild Type ◽

Anion Channels ◽

In The Wild

Abstract Cytosolic calcium ([Ca2+]cyt) elevation activates plasma membrane anion channels in guard cells, which is required for stomatal closure. However, involvement of the anion channels in the [Ca2+]cyt elevation remains unclear. We investigated the involvement using Arabidopsis thaliana anion channel mutants, slac1-4 slah3-3 and slac1-4 almt12-1. Extracellular calcium induced stomatal closure in the wild-type plants but not in the anion channel mutant plants whereas extracellular calcium induced [Ca2+]cyt elevation both in the wild-type guard cells and in the mutant guard cells. The peak height and the number of the [Ca2+]cyt spike were lower and larger in the slac1-4 slah3-3 than in the wild-type and the height and the number in the slac1-4 almt12-1 were much lower and much larger than in the wild-type. These results suggest that the anion channels are involved in the regulation of [Ca2+]cyt elevation in guard cells.

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Estimations of apoplastic concentrations of K+ and Ca2+ in the vicinity of stomatal guard cells

New Phytologist ◽

10.1111/j.1469-8137.1996.tb04363.x ◽

1996 ◽

Vol 134 (3) ◽

pp. 463-469 ◽

Cited By ~ 19

Author(s):

D. L. R. SILVA ◽

SARAH J. HONOUR ◽

T. A. MANSFIELD

Keyword(s):

Guard Cells ◽

Stomatal Guard Cells

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Submicroscopical Features of Leaves of Xyris Species

Brazilian Archives of Biology and Technology ◽

10.1590/s1516-89132001000400011 ◽

2001 ◽

Vol 44 (4) ◽

pp. 405-410 ◽

Cited By ~ 1

Author(s):

Maria das Graças Sajo ◽

Silvia Rodrigues Machado

Keyword(s):

Electron Microscope ◽

Cell Walls ◽

Guard Cells ◽

Leaf Ultrastructure ◽

Mesophyll Cells ◽

Transmission Electron ◽

Inner Surface ◽

Stomatal Guard Cells ◽

Adaptative Significance ◽

Scanning Electron

The leaf ultrastructure of five Xyris species were examined using scanning electron microscope (SEM), transmission electron microscope (TEM) and histochemical methods. All studied leaves show some features in epidermis and mesophyll, which were of considerable adaptative significance to drought stress. Such features included the occurrence of a pectic layer on the stomatal guard cells and the presence of a network of pectic compounds in the cuticle. Pectic compunds were also in abundance in lamellated walls of the mesophyll cells and on the inner surface of the sclerified cell walls of the vascular bundle sheaths. There were also specialized chlorenchymatous "peg cells" in the mesophyll and drops of phenolic compounds inside the epidermal cells.

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Evolution of chloroplast retrograde signaling facilitates green plant adaptation to land

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.1812092116 ◽

2019 ◽

Vol 116 (11) ◽

pp. 5015-5020 ◽

Cited By ~ 44

Author(s):

Chenchen Zhao ◽

Yuanyuan Wang ◽

Kai Xun Chan ◽

D. Blaine Marchant ◽

Peter J. Franks ◽

...

Keyword(s):

Drought Stress ◽

Physcomitrella Patens ◽

Stomatal Closure ◽

Guard Cells ◽

Green Plant ◽

Land Plants ◽

Retrograde Signaling ◽

Plant Adaptation ◽

Origin And Evolution ◽

Stomatal Regulation

Chloroplast retrograde signaling networks are vital for chloroplast biogenesis, operation, and signaling, including excess light and drought stress signaling. To date, retrograde signaling has been considered in the context of land plant adaptation, but not regarding the origin and evolution of signaling cascades linking chloroplast function to stomatal regulation. We show that key elements of the chloroplast retrograde signaling process, the nucleotide phosphatase (SAL1) and 3′-phosphoadenosine-5′-phosphate (PAP) metabolism, evolved in streptophyte algae—the algal ancestors of land plants. We discover an early evolution of SAL1-PAP chloroplast retrograde signaling in stomatal regulation based on conserved gene and protein structure, function, and enzyme activity and transit peptides of SAL1s in species including flowering plants, the fern Ceratopteris richardii, and the moss Physcomitrella patens. Moreover, we demonstrate that PAP regulates stomatal closure via secondary messengers and ion transport in guard cells of these diverse lineages. The origin of stomata facilitated gas exchange in the earliest land plants. Our findings suggest that the conquest of land by plants was enabled by rapid response to drought stress through the deployment of an ancestral SAL1-PAP signaling pathway, intersecting with the core abscisic acid signaling in stomatal guard cells.

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