Chloroplast NADH dehydrogenase‐like complex‐mediated cyclic electron flow is the main electron transport route in C4 bundle sheath cells

Summary The superior productivity of C4 plants is achieved via a metabolic C4 cycle which acts as a CO2 pump across mesophyll and bundle sheath (BS) cells and requires an additional input of energy in the form of ATP. The importance of chloroplast NADH dehydrogenase‐like complex (NDH) operating cycl...

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Bibliographic Details
Published in:The New phytologist 2024-09, Vol.243 (6), p.2187-2200
Main Authors: Ermakova, Maria, Woodford, Russell, Fitzpatrick, Duncan, Nix, Samuel J., Zwahlen, Soraya M., Farquhar, Graham D., Caemmerer, Susanne, Furbank, Robert T.
Format: Article
Language:English
Subjects:
Alleles
ATP
bundle sheath
C4 photosynthesis
Carbon dioxide
Carbon dioxide fixation
Carbon fixation
Cells
Chloroplasts
CO2 assimilation
cyclic electron flow
Dehydrogenase
Dehydrogenases
Electron flux
Electron transport
Gene flow
Genetics
gene‐editing
Mesophyll
NADH dehydrogenase
NDH complex
Nicotinamide adenine dinucleotide
Photosynthesis
Photosystem I
Plant cells
Plant growth
Plants (botany)
Sheaths
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Summary:Summary The superior productivity of C4 plants is achieved via a metabolic C4 cycle which acts as a CO2 pump across mesophyll and bundle sheath (BS) cells and requires an additional input of energy in the form of ATP. The importance of chloroplast NADH dehydrogenase‐like complex (NDH) operating cyclic electron flow (CEF) around Photosystem I (PSI) for C4 photosynthesis has been shown in reverse genetics studies but the contribution of CEF and NDH to cell‐level electron fluxes remained unknown. We have created gene‐edited Setaria viridis with null ndhO alleles lacking functional NDH and developed methods for quantification of electron flow through NDH in BS and mesophyll cells. We show that CEF accounts for 84% of electrons reducing PSI in BS cells and most of those electrons are delivered through NDH while the contribution of the complex to electron transport in mesophyll cells is minimal. A decreased leaf CO2 assimilation rate and growth of plants lacking NDH cannot be rescued by supplying additional CO2. Our results indicate that NDH‐mediated CEF is the primary electron transport route in BS chloroplasts highlighting the essential role of NDH in generating ATP required for CO2 fixation by the C3 cycle in BS cells.
ISSN:0028-646X
1469-8137
1469-8137
DOI:10.1111/nph.19982