Engineering a K+ channel ‘sensory antenna’ enhances stomatal kinetics, water use efficiency and photosynthesis

Horaruang, Wijitra; Klejchová, Martina; Carroll, William L.; Silva‐Alvim, Fernanda A. L.; Waghmare, Sakharam; Papanatsiou, Maria; Amtmann, Anna; Hills, Adrian; Alvim, Jonas Chaves; Blatt, Michael R.; Zhang, Ben

doi:10.1038/s41477-022-01255-2

Cited by 26 publications

(20 citation statements)

References 79 publications

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“…Values are steady-state means ± SE from n plants with individual measurements indicated by small symbols. Asterisks indicate significant differences (****p ≤ 0.0001) by post-hoc unpaired t test.from a conditioning voltage negative of E K to more positive values, yielded time-and voltage-dependent currents characteristic of outward-rectifying K + channels described previously(Blatt & Gradmann, 1997;Horaruang et al, 2022). As is typical of these channels, increasing external K + shifted the steady-state currentvoltage (I-V) curves to more positive voltages and slowed current activation at any one voltage (Figure4a,b).To assess the selectivity and [K + ] dependence of the channels, tail currents were analysed from G. gynandra guard cells by stepping to more negative voltages after activating the current.…”

mentioning

confidence: 78%

“…where V 1/2 and δ values were derived from joint fittings of the I-V curves to the Boltzmann function (Figure 4, Table 3). The comparison shows that the energy required for gating of the G. gynandra channel systems platform OnGuard3 (Horaruang et al, 2022;Jezek et al, 2021;Wang, Hills, et al, 2014;Wang, Noguchi, et al, 2014) and experiments in vivo (Horaruang et al, 2022) It is worth noting that the differences in gating of the outwardrectifying channels of G. gynandra and Arabidopsis almost certainly dominate over any differences in current amplitudes (Table 3;…”

Section: G Gynandra Maintains Lower and Faster Stomata Conductance Re...mentioning

confidence: 99%

“…Horaruang et al (2022) identified as critical to K + gating inhibition sets of alternating positive and negative charges within an intrinsically disordered region of the GORK N-terminus. This domain and charge alternations are conserved among a number of putative, outward-rectifying K + channels in the guard cells of C 3 species, including rice and wheat.…”

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confidence: 99%

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Speedy stomata of a C₄ plant correlate with enhanced K⁺ channel gating

Silva‐Alvim,

Alvim,

Harvey

et al. 2023

Plant Cell & Environment

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Stomata are microscopic pores at the surface of plant leaves that facilitate gaseous diffusion to support photosynthesis. The guard cells around each stoma regulate the pore aperture. Plants that carry out C4 photosynthesis are usually more resilient than C3 plants to stress, and their stomata operate over a lower dynamic range of CO2 within the leaf. What makes guard cells of C4 plants more responsive than those of C3 plants? We used gas exchange and electrophysiology, comparing stomatal kinetics of the C4 plant Gynandropsis gynandra and the phylogenetically related C3 plant Arabidopsis thaliana. We found, with varying CO2 and light, that Gynandropsis showed faster changes in stomata conductance and greater water use efficiency when compared with Arabidopsis. Electrophysiological analysis of the dominant K+ channels showed that the outward‐rectifying channels, responsible for K+ loss during stomatal closing, were characterised by a greater maximum conductance and substantial negative shift in the voltage dependence of gating, indicating a reduced inhibition by extracellular K+ and enhanced capacity for K+ flux. These differences correlated with the accelerated stomata kinetics of Gynandropsis, suggesting that subtle changes in the biophysical properties of a key transporter may prove a target for future efforts to engineer C4 stomatal kinetics.

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confidence: 78%

Section: G Gynandra Maintains Lower and Faster Stomata Conductance Re...mentioning

confidence: 99%

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Speedy stomata of a C₄ plant correlate with enhanced K⁺ channel gating

Silva‐Alvim,

Alvim,

Harvey

et al. 2023

Plant Cell & Environment

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“…How gating in GORK and its homologs is coupled with extracellular K + remains a matter of interest, not least because it is likely to underpin the rapid stomatal movements of many plants with C 4 photosynthesis ( Alvim 2022 ) and has implications for the channel protein dynamics ( Eisenach et al 2014 ). My laboratory recently found that manipulating this coupling yields substantial gains in both water use efficiency and photosynthetic carbon assimilation when light fluctuates, as it commonly does in the environment ( Blatt and Alvim 2022 ; Horaruang et al 2022 ).…”

Section: The Guard Cell Modelmentioning

confidence: 99%

A charged existence: A century of transmembrane ion transport in plants

Blatt

2024

Plant Physiology

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If the past century marked the birth of membrane transport as a focus for research in plants, the past 50 years has seen the field mature from arcane interest to a central pillar of plant physiology. Ion transport across plant membranes accounts for roughly 30% of the metabolic energy consumed by a plant cell, and it underpins virtually every aspect of plant biology, from mineral nutrition, cell expansion, and development to auxin polarity, fertilization, plant pathogen defense, and senescence. The means to quantify ion flux through individual transporters, even single channel proteins, became widely available as voltage clamp methods expanded from giant algal cells to the fungus Neurospora crassa in the 1970s and the cells of angiosperms in the 1980s. Here, I touch briefly on some key aspects of the development of modern electrophysiology with a focus on the guard cells of stomata, now without dispute the premier plant cell model for ion transport and its regulation. Guard cells have proven to be a crucible for many technical and conceptual developments that have since emerged into the mainstream of plant science. Their study continues to provide fundamental insights and carries much importance for the global challenges that face us today.

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“…Most recently, OnGuard3 was used to guide the engineering of a guard cell ion channel for improved WUE and biomass gains (Horaruang et al, 2022).…”

Section: Inside the Onguard3e Platformmentioning

confidence: 99%

OnGuard3e: A predictive, ecophysiology‐ready tool for gas exchange and photosynthesis research

Nguyen

Silva‐Alvim

Hills

et al. 2023

Plant Cell & Environment

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Gas exchange across the stomatal pores of leaves is a focal point in studies of plant‐environmental relations. Stomata regulate atmospheric exchange with the inner air spaces of the leaf. They open to allow CO2 entry for photosynthesis and close to minimize water loss. Models that focus on the phenomenology of stomatal conductance generally omit the mechanics of the guard cells that regulate the pore aperture. The OnGuard platform fills this gap and offers a truly mechanistic approach with which to analyse stomatal gas exchange, whole‐plant carbon assimilation and water‐use efficiency. Previously, OnGuard required specialist knowledge of membrane transport, signalling and metabolism. Here we introduce OnGuard3e, a software package accessible to ecophysiologists and membrane biologists alike. We provide a brief guide to its use and illustrate how the package can be applied to explore and analyse stomatal conductance, assimilation and water use efficiencies, addressing a range of experimental questions with truly predictive outputs.

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Engineering a K+ channel ‘sensory antenna’ enhances stomatal kinetics, water use efficiency and photosynthesis

Abstract: K + channel / ion channel clustering / channel gating, K + dependent / photosynthesis / stomatal gas exchange / Arabidopsis

Cited by 26 publications

References 79 publications

Speedy stomata of a C₄ plant correlate with enhanced K⁺ channel gating

Speedy stomata of a C₄ plant correlate with enhanced K⁺ channel gating

A charged existence: A century of transmembrane ion transport in plants

OnGuard3e: A predictive, ecophysiology‐ready tool for gas exchange and photosynthesis research

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Engineering a K+ channel ‘sensory antenna’ enhances stomatal kinetics, water use efficiency and photosynthesis

Abstract: K + channel / ion channel clustering / channel gating, K + dependent / photosynthesis / stomatal gas exchange / Arabidopsis

Cited by 26 publications

References 79 publications

Speedy stomata of a C4 plant correlate with enhanced K+ channel gating

Speedy stomata of a C4 plant correlate with enhanced K+ channel gating

A charged existence: A century of transmembrane ion transport in plants

OnGuard3e: A predictive, ecophysiology‐ready tool for gas exchange and photosynthesis research

Contact Info

Product

Resources

About

Speedy stomata of a C₄ plant correlate with enhanced K⁺ channel gating

Speedy stomata of a C₄ plant correlate with enhanced K⁺ channel gating