K+ and Cl− channels/transporters independently fine-tune photosynthesis in plants

Emilija Dukic; Andrei Herdean; Otilia Cheregi; Anurag Sharma; Hugues Nziengui; Dominika Dmitruk; Katalin Solymosi; Mathias Pribil; Cornelia Spetea

doi:10.1038/s41598-019-44972-z

K⁺ and Cl⁻ channels/transporters independently fine-tune photosynthesis in plants

Emilija Dukic, Andrei Herdean, Otilia Cheregi, Anurag Sharma, Hugues Nziengui, Dominika Dmitruk, Katalin Solymosi, Mathias Pribil, Cornelia Spetea^*

^*Corresponding author for this work

10 Citations (Scopus)

19 Downloads (Pure)

Abstract

In variable light environments, plants adjust light use in photosynthetic electron transport and photoprotective dissipation in the thylakoid membrane. In this respect, roles of the K⁺/H⁺ antiporter KEA3, the Cl⁻ channel/transporter CLCe and the voltage-dependent Cl⁻ channel VCCN1 have been unraveled in Arabidopsis thaliana. Here we report that they independently adjust photosynthesis on the basis of analyses using single and higher order loss-of-function mutants. In short experiments of photosynthetic response on transition from dark to low light, we reveal a sequential functioning of VCCN1 and CLCe in the activation of photoprotection and of KEA3 in its downregulation to a low steady state while adjusting the electron transport. On transition from low to high light, VCCN1 accelerates the activation of photoprotection, whereas KEA3 slows it down on transition from high to low light. Based on parallel electrochromic band shift measurements, the mechanism behind is that VCCN1 builds up a pH gradient across the thylakoid membrane, whereas KEA3 dissipates this gradient, which affects photoprotection. CLCe regulates photosynthesis by a pH-independent mechanism likely involving Cl⁻ homeostasis. Nevertheless, all genotypes grow well in alternating high and low light. Taken together, the three studied ion channels/transporters function independently in adjusting photosynthesis to the light environment.

Original language	English
Article number	8639
Journal	Scientific Reports
Volume	9
Pages (from-to)	1-12
ISSN	2045-2322
DOIs	https://doi.org/10.1038/s41598-019-44972-z
Publication status	Published - 2019

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K+ and Cl− channels/transporters independently fine-tune photosynthesis in plantsFinal published version, 4.17 MBLicence: CC BY

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title = "K+ and Cl− channels/transporters independently fine-tune photosynthesis in plants",

abstract = "In variable light environments, plants adjust light use in photosynthetic electron transport and photoprotective dissipation in the thylakoid membrane. In this respect, roles of the K+/H+ antiporter KEA3, the Cl− channel/transporter CLCe and the voltage-dependent Cl− channel VCCN1 have been unraveled in Arabidopsis thaliana. Here we report that they independently adjust photosynthesis on the basis of analyses using single and higher order loss-of-function mutants. In short experiments of photosynthetic response on transition from dark to low light, we reveal a sequential functioning of VCCN1 and CLCe in the activation of photoprotection and of KEA3 in its downregulation to a low steady state while adjusting the electron transport. On transition from low to high light, VCCN1 accelerates the activation of photoprotection, whereas KEA3 slows it down on transition from high to low light. Based on parallel electrochromic band shift measurements, the mechanism behind is that VCCN1 builds up a pH gradient across the thylakoid membrane, whereas KEA3 dissipates this gradient, which affects photoprotection. CLCe regulates photosynthesis by a pH-independent mechanism likely involving Cl− homeostasis. Nevertheless, all genotypes grow well in alternating high and low light. Taken together, the three studied ion channels/transporters function independently in adjusting photosynthesis to the light environment.",

author = "Emilija Dukic and Andrei Herdean and Otilia Cheregi and Anurag Sharma and Hugues Nziengui and Dominika Dmitruk and Katalin Solymosi and Mathias Pribil and Cornelia Spetea",

year = "2019",

doi = "10.1038/s41598-019-44972-z",

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AU - Dukic, Emilija

AU - Herdean, Andrei

AU - Cheregi, Otilia

AU - Sharma, Anurag

AU - Nziengui, Hugues

AU - Dmitruk, Dominika

AU - Solymosi, Katalin

AU - Pribil, Mathias

AU - Spetea, Cornelia

PY - 2019

Y1 - 2019

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AB - In variable light environments, plants adjust light use in photosynthetic electron transport and photoprotective dissipation in the thylakoid membrane. In this respect, roles of the K+/H+ antiporter KEA3, the Cl− channel/transporter CLCe and the voltage-dependent Cl− channel VCCN1 have been unraveled in Arabidopsis thaliana. Here we report that they independently adjust photosynthesis on the basis of analyses using single and higher order loss-of-function mutants. In short experiments of photosynthetic response on transition from dark to low light, we reveal a sequential functioning of VCCN1 and CLCe in the activation of photoprotection and of KEA3 in its downregulation to a low steady state while adjusting the electron transport. On transition from low to high light, VCCN1 accelerates the activation of photoprotection, whereas KEA3 slows it down on transition from high to low light. Based on parallel electrochromic band shift measurements, the mechanism behind is that VCCN1 builds up a pH gradient across the thylakoid membrane, whereas KEA3 dissipates this gradient, which affects photoprotection. CLCe regulates photosynthesis by a pH-independent mechanism likely involving Cl− homeostasis. Nevertheless, all genotypes grow well in alternating high and low light. Taken together, the three studied ion channels/transporters function independently in adjusting photosynthesis to the light environment.

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K⁺ and Cl⁻ channels/transporters independently fine-tune photosynthesis in plants

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