Promotion and Upregulation of a Plasma Membrane Proton-ATPase Strategy: Principles and Applications

Plasma membrane proton-ATPase (PM H+-ATPase) is a primary H+ transporter that consumes ATP in vivo and is a limiting factor in the blue light-induced stomatal opening signaling pathway. It was recently reported that manipulation of PM H+-ATPase in stomatal guard cells and other tissues greatly improved leaf photosynthesis and plant growth. In this report, we review and discuss the function of PM H+-ATPase in the context of the promotion and upregulation H+-ATPase strategy, including associated principles pertaining to enhanced stomatal opening, environmental plasticity, and potential applications in crops and nanotechnology. We highlight the great potential of the promotion and upregulation H+-ATPase strategy, and explain why it may be applied in many crops in the future.

Download Full-text

Anion channel sensitivity to cytosolic organic acids implicates a central role for oxaloacetate in integrating ion flux with metabolism in stomatal guard cells

Biochemical Journal ◽

10.1042/bj20110845 ◽

2011 ◽

Vol 439 (1) ◽

pp. 161-170 ◽

Cited By ~ 20

Author(s):

Yizhou Wang ◽

Michael R. Blatt

Keyword(s):

Plasma Membrane ◽

Organic Acids ◽

Organic Acid ◽

Stomatal Closure ◽

Anion Channel ◽

Guard Cells ◽

Solute Flux ◽

Stomatal Guard Cells ◽

The Impact

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.

Download Full-text

Overexpression of plasma membrane H+-ATPase in guard cells promotes light-induced stomatal opening and enhances plant growth

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.1305438111 ◽

2013 ◽

Vol 111 (1) ◽

pp. 533-538 ◽

Cited By ~ 95

Author(s):

Y. Wang ◽

K. Noguchi ◽

N. Ono ◽

S.-i. Inoue ◽

I. Terashima ◽

...

Keyword(s):

Plasma Membrane ◽

Plant Growth ◽

Guard Cells ◽

Stomatal Opening

Download Full-text

Faculty Opinions recommendation of Overexpression of plasma membrane H+-ATPase in guard cells promotes light-induced stomatal opening and enhances plant growth.

Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature ◽

10.3410/f.718216302.793489520 ◽

2014 ◽

Author(s):

Ekkehard Neuhaus

Keyword(s):

Plasma Membrane ◽

Plant Growth ◽

Guard Cells ◽

Stomatal Opening

Download Full-text

Overexpression of Plasma Membrane H+-ATPase in Guard Cells Enhances Light-Induced Stomatal Opening, Photosynthesis, and Plant Growth in Hybrid Aspen

Frontiers in Plant Science ◽

10.3389/fpls.2021.766037 ◽

2021 ◽

Vol 12 ◽

Author(s):

Shigeo Toh ◽

Naoki Takata ◽

Eigo Ando ◽

Yosuke Toda ◽

Yin Wang ◽

...

Keyword(s):

Plasma Membrane ◽

Transgenic Plants ◽

Woody Plants ◽

Stem Elongation ◽

Guard Cells ◽

Gus Expression ◽

Stomatal Opening ◽

Wild Type ◽

Exchange System ◽

Gas Exchange System

Stomata in the plant epidermis open in response to light and regulate CO2 uptake for photosynthesis and transpiration for uptake of water and nutrients from roots. Light-induced stomatal opening is mediated by activation of the plasma membrane (PM) H+-ATPase in guard cells. Overexpression of PM H+-ATPase in guard cells promotes light-induced stomatal opening, enhancing photosynthesis and growth in Arabidopsis thaliana. In this study, transgenic hybrid aspens overexpressing Arabidopsis PM H+-ATPase (AHA2) in guard cells under the strong guard cell promoter Arabidopsis GC1 (AtGC1) showed enhanced light-induced stomatal opening, photosynthesis, and growth. First, we confirmed that AtGC1 induces GUS expression specifically in guard cells in hybrid aspens. Thus, we produced AtGC1::AHA2 transgenic hybrid aspens and confirmed expression of AHA2 in AtGC1::AHA2 transgenic plants. In addition, AtGC1::AHA2 transgenic plants showed a higher PM H+-ATPase protein level in guard cells. Analysis using a gas exchange system revealed that transpiration and the photosynthetic rate were significantly increased in AtGC1::AHA2 transgenic aspen plants. AtGC1::AHA2 transgenic plants showed a>20% higher stem elongation rate than the wild type (WT). Therefore, overexpression of PM H+-ATPase in guard cells promotes the growth of perennial woody plants.

Download Full-text

Immunohistochemical Detection of Blue Light-Induced Phosphorylation of the Plasma Membrane H+-ATPase in Stomatal Guard Cells

Plant and Cell Physiology ◽

10.1093/pcp/pcr072 ◽

2011 ◽

Vol 52 (7) ◽

pp. 1238-1248 ◽

Cited By ~ 61

Author(s):

Maki Hayashi ◽

Shin-ichiro Inoue ◽

Koji Takahashi ◽

Toshinori Kinoshita

Keyword(s):

Plasma Membrane ◽

Blue Light ◽

Guard Cells ◽

Immunohistochemical Detection ◽

Stomatal Guard Cells

Download Full-text

Raf-like kinases CBC1 and CBC2 negatively regulate stomatal opening by negatively regulating plasma membrane H+-ATPase phosphorylation in Arabidopsis

Photochemical & Photobiological Sciences ◽

10.1039/c9pp00329k ◽

2020 ◽

Vol 19 (1) ◽

pp. 88-98 ◽

Cited By ~ 2

Author(s):

Maki Hayashi ◽

Hodaka Sugimoto ◽

Hirotaka Takahashi ◽

Motoaki Seki ◽

Kazuo Shinozaki ◽

...

Keyword(s):

Plasma Membrane ◽

Blue Light ◽

Guard Cells ◽

Stomatal Opening

Raf-like kinases CBC1 and CBC2 negatively regulate phosphorylation of plasma membrane H+-ATPase in guard cells and blue light-dependent stomatal opening.

Download Full-text

Blue light activates the plasma membrane H+-ATPase by phosphorylation of the C-terminus in stomatal guard cells

The EMBO Journal ◽

10.1093/emboj/18.20.5548 ◽

1999 ◽

Vol 18 (20) ◽

pp. 5548-5558 ◽

Cited By ~ 259

Author(s):

T. Kinoshita

Keyword(s):

Plasma Membrane ◽

Blue Light ◽

Guard Cells ◽

C Terminus ◽

Stomatal Guard Cells

Download Full-text

Identification of Genes Preferentially Expressed in Stomatal Guard Cells of Arabidopsis thaliana and Involvement of the Aluminum-Activated Malate Transporter 6 Vacuolar Malate Channel in Stomatal Opening

Frontiers in Plant Science ◽

10.3389/fpls.2021.744991 ◽

2021 ◽

Vol 12 ◽

Author(s):

Wenxiu Ye ◽

Shota Koya ◽

Yuki Hayashi ◽

Huimin Jiang ◽

Takaya Oishi ◽

...

Keyword(s):

Guard Cells ◽

Stomatal Opening ◽

Stomatal Movement ◽

Null Mutant ◽

Reverse Transcription Pcr ◽

Public Resources ◽

Stomatal Guard Cells ◽

Signaling Components ◽

Malate Transporter ◽

Gdsl Lipase

Stomatal guard cells (GCs) are highly specialized cells that respond to various stimuli, such as blue light (BL) and abscisic acid, for the regulation of stomatal aperture. Many signaling components that are involved in the stomatal movement are preferentially expressed in GCs. In this study, we identified four new such genes in addition to an aluminum-activated malate transporter, ALMT6, and GDSL lipase, Occlusion of Stomatal Pore 1 (OSP1), based on the expression analysis using public resources, reverse transcription PCR, and promoter-driven β-glucuronidase assays. Some null mutants of GC-specific genes evidenced altered stomatal movement. We further investigated the role played by ALMT6, a vacuolar malate channel, in stomatal opening. Epidermal strips from an ALMT6-null mutant exhibited defective stomatal opening induced by BL and fusicoccin, a strong plasma membrane H+-ATPase activator. The deficiency was enhanced when the assay buffer [Cl–] was low, suggesting that malate and/or Cl– facilitate efficient opening. The results indicate that the GC-specific genes are frequently involved in stomatal movement. Further detailed analyses of the hitherto uncharacterized GC-specific genes will provide new insights into stomatal regulation.

Download Full-text