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Cyclosis-mediated transport and redox regulation of chloroplast activity probed by local microinjection in characean alga.

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Title: Cyclosis-mediated transport and redox regulation of chloroplast activity probed by local microinjection in characean alga.
Authors: Krupenina NA; Faculty of Biology, Lomonosov Moscow State University, Moscow, Russia. Electronic address: kamzolkina-n@yandex.ru., Bulychev AA; Faculty of Biology, Lomonosov Moscow State University, Moscow, Russia. Electronic address: bulychev@biophys.msu.ru., Alova AV; Faculty of Biology, Lomonosov Moscow State University, Moscow, Russia., von Ruling F; Faculty of Natural Sciences, Otto von Guericke University, Magdeburg, Germany., Eremin A; Faculty of Natural Sciences, Otto von Guericke University, Magdeburg, Germany.
Source: Biochimica et biophysica acta. Bioenergetics [Biochim Biophys Acta Bioenerg] 2026 Aug 01; Vol. 1867 (3), pp. 149589. Date of Electronic Publication: 2026 Mar 21.
Publication Type: Journal Article
Language: English
Journal Info: Publisher: Elsevier Country of Publication: Netherlands NLM ID: 101731706 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1879-2650 (Electronic) Linking ISSN: 00052728 NLM ISO Abbreviation: Biochim Biophys Acta Bioenerg Subsets: MEDLINE
Imprint Name(s): Original Publication: Amsterdam : Elsevier
MeSH Terms: Chloroplasts*/metabolism , Chara*/metabolism, Hydrogen Peroxide/metabolism ; Hydrogen Peroxide/pharmacology ; NAD/metabolism ; Chlorophyll/metabolism ; Oxidation-Reduction ; Microinjections ; Photosynthesis ; Electron Transport ; Biological Transport ; Cytoplasmic Streaming ; Light
Abstract: Internodal cells of Characeae exposed to flickering spotted illumination mobilize long-range interchloroplast communications between the point of local light stress and non-treated cell areas. The signaling and functional coordination between immobile chloroplasts involves the export of excess products from light-stressed plastids, the lateral transport by the streaming cytoplasm, the entry of delivered substances to dimly lit recipient chloroplasts, and metabolic responses to the entered agents. There is indirect evidence that interchloroplast communications are mediated by two types of metabolites produced during photosynthetic electron transport: reducing agents such as NAD(P)H and the product of oxygen reduction H2O2 as the most stable ROS form. The involvement of these substances in intracellular signaling was tested in this study using local extracellular application of subnanomolar quantities of H2O2 and the cytoplasmic microinjection of NADH in combination with Microscopy-PAM chlorophyll fluorometry and confocal laser scanning microscopy. The pointed introduction of the above agents affected the actual and maximal chlorophyll (Chl) fluorescence yields (F' and Fm') in chloroplasts exposed to dim background light but had no effect in darkened cells. The Chl fluorescence changes induced by NADH and H2O2 featured opposite polarities, indicating the plastoquinone reduction (via segments of cyclic electron-transport pathways) and the development of non-photochemical quenching, respectively. The ability of externally applied H2O2 to move with the cytoplasmic flow has been revealed; it confirms that H2O2 can act in plant cells as a transportable signaling substance. The results provide evidence for participation of reducing substances and the oxidizing agent H2O2 in interchloroplast communications.
(Copyright © 2026 Elsevier B.V. All rights reserved.)
Competing Interests: Declaration of competing interest The authors declare the following financial interests/personal relationships which may be considered as potential competing interests: Alexei Eremin reports financial support was provided by Deutsche Forschungsgemeinschaft. Alexander Bulychev, Anna Alova reports a relationship with Russian Foundation for Basic Research that includes: funding grants. If there are other authors, they declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Contributed Indexing: Keywords: Chara australis; Chloroplast envelope; Cytoplasmic streaming; Light-dependent transporters; Microfluidic signaling; Microinjection; NADH and H(2)O(2) effects on photosynthetic electron transport
Substance Nomenclature: BBX060AN9V (Hydrogen Peroxide)
0U46U6E8UK (NAD)
1406-65-1 (Chlorophyll)
Entry Date(s): Date Created: 20260323 Date Completed: 20260613 Latest Revision: 20260613
Update Code: 20260615
DOI: 10.1016/j.bbabio.2026.149589
PMID: 41871708
Database: MEDLINE
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  Data: Cyclosis-mediated transport and redox regulation of chloroplast activity probed by local microinjection in characean alga.
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  Data: <searchLink fieldCode="AU" term="%22Krupenina+NA%22">Krupenina NA</searchLink>; Faculty of Biology, Lomonosov Moscow State University, Moscow, Russia. Electronic address: kamzolkina-n@yandex.ru.<br /><searchLink fieldCode="AU" term="%22Bulychev+AA%22">Bulychev AA</searchLink>; Faculty of Biology, Lomonosov Moscow State University, Moscow, Russia. Electronic address: bulychev@biophys.msu.ru.<br /><searchLink fieldCode="AU" term="%22Alova+AV%22">Alova AV</searchLink>; Faculty of Biology, Lomonosov Moscow State University, Moscow, Russia.<br /><searchLink fieldCode="AU" term="%22von+Ruling+F%22">von Ruling F</searchLink>; Faculty of Natural Sciences, Otto von Guericke University, Magdeburg, Germany.<br /><searchLink fieldCode="AU" term="%22Eremin+A%22">Eremin A</searchLink>; Faculty of Natural Sciences, Otto von Guericke University, Magdeburg, Germany.
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  Data: <searchLink fieldCode="JN" term="%22101731706%22">Biochimica et biophysica acta. Bioenergetics</searchLink> [Biochim Biophys Acta Bioenerg] 2026 Aug 01; Vol. 1867 (3), pp. 149589. <i>Date of Electronic Publication: </i>2026 Mar 21.
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  Data: <i>Publisher: </i><searchLink fieldCode="PB" term="%22Elsevier%22">Elsevier </searchLink><i>Country of Publication: </i>Netherlands <i>NLM ID: </i>101731706 <i>Publication Model: </i>Print-Electronic <i>Cited Medium: </i>Internet <i>ISSN: </i>1879-2650 (Electronic) <i>Linking ISSN: </i><searchLink fieldCode="IS" term="%2200052728%22">00052728 </searchLink><i>NLM ISO Abbreviation: </i>Biochim Biophys Acta Bioenerg <i>Subsets: </i>MEDLINE
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  Data: <i>Original Publication</i>: Amsterdam : Elsevier
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  Data: <searchLink fieldCode="MM" term="%22Chloroplasts%22">Chloroplasts*</searchLink>/<searchLink fieldCode="MM" term="%22Chloroplasts+metabolism%22">metabolism</searchLink> <br /><searchLink fieldCode="MM" term="%22Chara%22">Chara*</searchLink>/<searchLink fieldCode="MM" term="%22Chara+metabolism%22">metabolism</searchLink><br /><searchLink fieldCode="MH" term="%22Hydrogen+Peroxide%22">Hydrogen Peroxide</searchLink>/<searchLink fieldCode="MH" term="%22Hydrogen+Peroxide+metabolism%22">metabolism</searchLink> ; <searchLink fieldCode="MH" term="%22Hydrogen+Peroxide%22">Hydrogen Peroxide</searchLink>/<searchLink fieldCode="MH" term="%22Hydrogen+Peroxide+pharmacology%22">pharmacology</searchLink> ; <searchLink fieldCode="MH" term="%22NAD%22">NAD</searchLink>/<searchLink fieldCode="MH" term="%22NAD+metabolism%22">metabolism</searchLink> ; <searchLink fieldCode="MH" term="%22Chlorophyll%22">Chlorophyll</searchLink>/<searchLink fieldCode="MH" term="%22Chlorophyll+metabolism%22">metabolism</searchLink> ; <searchLink fieldCode="MH" term="%22Oxidation-Reduction%22">Oxidation-Reduction</searchLink> ; <searchLink fieldCode="MH" term="%22Microinjections%22">Microinjections</searchLink> ; <searchLink fieldCode="MH" term="%22Photosynthesis%22">Photosynthesis</searchLink> ; <searchLink fieldCode="MH" term="%22Electron+Transport%22">Electron Transport</searchLink> ; <searchLink fieldCode="MH" term="%22Biological+Transport%22">Biological Transport</searchLink> ; <searchLink fieldCode="MH" term="%22Cytoplasmic+Streaming%22">Cytoplasmic Streaming</searchLink> ; <searchLink fieldCode="MH" term="%22Light%22">Light</searchLink>
– Name: Abstract
  Label: Abstract
  Group: Ab
  Data: Internodal cells of Characeae exposed to flickering spotted illumination mobilize long-range interchloroplast communications between the point of local light stress and non-treated cell areas. The signaling and functional coordination between immobile chloroplasts involves the export of excess products from light-stressed plastids, the lateral transport by the streaming cytoplasm, the entry of delivered substances to dimly lit recipient chloroplasts, and metabolic responses to the entered agents. There is indirect evidence that interchloroplast communications are mediated by two types of metabolites produced during photosynthetic electron transport: reducing agents such as NAD(P)H and the product of oxygen reduction H<subscript>2</subscript>O<subscript>2</subscript> as the most stable ROS form. The involvement of these substances in intracellular signaling was tested in this study using local extracellular application of subnanomolar quantities of H<subscript>2</subscript>O<subscript>2</subscript> and the cytoplasmic microinjection of NADH in combination with Microscopy-PAM chlorophyll fluorometry and confocal laser scanning microscopy. The pointed introduction of the above agents affected the actual and maximal chlorophyll (Chl) fluorescence yields (F' and F<subscript>m</subscript>') in chloroplasts exposed to dim background light but had no effect in darkened cells. The Chl fluorescence changes induced by NADH and H<subscript>2</subscript>O<subscript>2</subscript> featured opposite polarities, indicating the plastoquinone reduction (via segments of cyclic electron-transport pathways) and the development of non-photochemical quenching, respectively. The ability of externally applied H<subscript>2</subscript>O<subscript>2</subscript> to move with the cytoplasmic flow has been revealed; it confirms that H<subscript>2</subscript>O<subscript>2</subscript> can act in plant cells as a transportable signaling substance. The results provide evidence for participation of reducing substances and the oxidizing agent H<subscript>2</subscript>O<subscript>2</subscript> in interchloroplast communications.<br /> (Copyright © 2026 Elsevier B.V. All rights reserved.)
– Name: Abstract
  Label: Competing Interests
  Group: Ab
  Data: Declaration of competing interest The authors declare the following financial interests/personal relationships which may be considered as potential competing interests: Alexei Eremin reports financial support was provided by Deutsche Forschungsgemeinschaft. Alexander Bulychev, Anna Alova reports a relationship with Russian Foundation for Basic Research that includes: funding grants. If there are other authors, they declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
– Name: SubjectMinor
  Label: Contributed Indexing
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  Data: <i>Keywords: </i>Chara australis; Chloroplast envelope; Cytoplasmic streaming; Light-dependent transporters; Microfluidic signaling; Microinjection; NADH and H(2)O(2) effects on photosynthetic electron transport
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  Data: BBX060AN9V (Hydrogen Peroxide)<br />0U46U6E8UK (NAD)<br />1406-65-1 (Chlorophyll)
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        Value: 10.1016/j.bbabio.2026.149589
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      – Code: eng
        Text: English
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        StartPage: 149589
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      – SubjectFull: Hydrogen Peroxide metabolism
        Type: general
      – SubjectFull: Hydrogen Peroxide pharmacology
        Type: general
      – SubjectFull: NAD metabolism
        Type: general
      – SubjectFull: Chlorophyll metabolism
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      – SubjectFull: Chloroplasts metabolism
        Type: general
      – SubjectFull: Chara metabolism
        Type: general
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      – TitleFull: Cyclosis-mediated transport and redox regulation of chloroplast activity probed by local microinjection in characean alga.
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