Effects of cell excitation on photosynthetic electron flow and intercellular transport in Chara.
Fluidic transport of metabolites
Membrane excitability
Plasmodesmata
Pulse-modulated chlorophyll microfluorometry
Journal
Protoplasma
ISSN: 1615-6102
Titre abrégé: Protoplasma
Pays: Austria
ID NLM: 9806853
Informations de publication
Date de publication:
Jan 2023
Jan 2023
Historique:
received:
16
12
2021
accepted:
14
02
2022
pubmed:
29
4
2022
medline:
10
1
2023
entrez:
28
4
2022
Statut:
ppublish
Résumé
Impact of membrane excitability on fluidic transport of photometabolites and their cell-to-cell passage via plasmodesmata was examined by pulse-modulated chlorophyll (Chl) microfluorometry in Chara australis internodes exposed to dim background light. The cells were subjected to a series of local light (LL) pulses with a 3-min period and a 30-s pulse width, which induced Chl fluorescence transients propagating in the direction of cytoplasmic streaming along the photostimulated and the neighboring internodes. By comparing Chl fluorescence changes induced in the LL-irradiated and the adjoining internodes, the permeability of the nodal complex for the photometabolites was assessed in the resting state and after the action potential (AP) generation. The electrically induced AP had no influence on Chl fluorescence in noncalcified cell regions but disturbed temporarily the metabolite transport along the internode and caused a disproportionally strong inhibition of intercellular metabolite transmission. In chloroplasts located close to calcified zones, Chl fluorescence increased transiently after cell excitation, which indicated the deceleration of photosynthetic electron flow on the acceptor side of photosystem I. Functional distinctions of chloroplasts located in noncalcified and calcified cell areas were also manifested in different modes of LL-induced changes of Chl fluorescence, which were accompanied by dissimilar changes in efficiency of PSII-driven electron flow. We conclude that chloroplasts located near the encrusted areas and in the incrustation-free cell regions are functionally distinct even in the absence of large-scale variations of cell surface pH. The inhibition of transnodal transport after AP generation is probably due to Ca
Identifiants
pubmed: 35482255
doi: 10.1007/s00709-022-01747-0
pii: 10.1007/s00709-022-01747-0
doi:
Substances chimiques
Chlorophyll
1406-65-1
Photosystem II Protein Complex
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
131-143Subventions
Organisme : Deutsche Forschungsgemeinschaft
ID : ER 467/14-1
Organisme : State Order of the Government of Russian Federation to Lomonosov Moscow State University
ID : 121032500058-7
Informations de copyright
© 2022. The Author(s), under exclusive licence to Springer-Verlag GmbH Austria, part of Springer Nature.
Références
Behera S, Xu Z, Luoni L, Bonza MC, Doccula FG, De Michelis MI, Morris RJ, Schwarzländer M, Costa A (2018) Cellular Ca
doi: 10.1105/tpc.18.00655
Beilby MJ (2016) Multi-scale characean experimental system: from electrophysiology of membrane transporters to cell-to-cell connectivity, cytoplasmic streaming and auxin metabolism. Front Plant Sci 7:1–20. https://doi.org/10.3389/fpls.2016.01052
doi: 10.3389/fpls.2016.01052
Berestovsky GN, Kataev AA (2005) Voltage-gated calcium and Ca
doi: 10.1007/s00249-005-0477-9
Bisson MA, Walker NA (1980) The Chara plasmalemma at high pH. Electrical measurements show rapid specific passive uniport of H
doi: 10.1007/BF01869346
Bulychev AA, Kamzolkina NA, Luengviriya J et al (2004) Effect of a single excitation stimulus on photosynthetic activity and light-dependent pH banding in Chara cells. J Membr Biol 202:11–19. https://doi.org/10.1007/s00232-004-0716-5
doi: 10.1007/s00232-004-0716-5
Bulychev AA, Kamzolkina NA (2006) Differential effects of plasma membrane electric excitation on H
doi: 10.1016/j.bioelechem.2006.03.001
Bulychev AA, Komarova AV (2015) Photoinduction of cyclosis-mediated interactions between distant chloroplasts. Biochim Biophys Acta - Bioenerg 1847:379–389. https://doi.org/10.1016/j.bbabio.2015.01.004
doi: 10.1016/j.bbabio.2015.01.004
Bulychev AA, Komarova AV (2017) Photoregulation of photosystem II activity mediated by cytoplasmic streaming in Chara and its relation to pH bands. Biochim Biophys Acta - Bioenerg 1858:386–395. https://doi.org/10.1016/j.bbabio.2017.02.014
doi: 10.1016/j.bbabio.2017.02.014
Bulychev AA, Rybina AA (2018) Long-range interactions of Chara chloroplasts are sensitive to plasma-membrane H
doi: 10.1007/s00709-018-1255-8
Bulychev AA (2019) Cyclosis-mediated intercellular transmission of photosynthetic metabolites in Chara revealed with chlorophyll microfluorometry. Protoplasma 256:815–826. https://doi.org/10.1007/s00709-018-01344-0
doi: 10.1007/s00709-018-01344-0
Bulychev AA, Krupenina NA (2019) Interchloroplast communications in Chara are suppressed under the alkaline bands and are relieved after the plasma membrane excitation. Bioelectrochemistry 129:62–69. https://doi.org/10.1016/j.bioelechem.2019.05.006
doi: 10.1016/j.bioelechem.2019.05.006
Bulychev AA, Cherkashin AA, Shapiguzov SY, Alova AV (2021) Effects of chloroplast–cytoplasm exchange and lateral mass transfer on slow induction of chlorophyll fluorescence in Characeae. Physiol Plant 173:1901–1913. https://doi.org/10.1111/ppl.13531
doi: 10.1111/ppl.13531
Cejudo FJ, González MC, Pérez-Ruiz JM (2021) Redox regulation of chloroplast metabolism. Plant Physiol 186:9–21. https://doi.org/10.1093/plphys/kiaa062
doi: 10.1093/plphys/kiaa062
Cleland RE, Fujiwara T, Lucas WJ (1994) Plasmodesmal-mediated cell-to-cell transport in wheat roots is modulated by anaerobic stress. Protoplasma 178:81–85. https://doi.org/10.1007/BF01404123
doi: 10.1007/BF01404123
Dmitrieva VA, Domashkina VV, Ivanova AN et al (2021) Regulation of plasmodesmata in Arabidopsis leaves: ATP, NADPH and chlorophyll b levels matter. J Exp Bot 72:5534–5552. https://doi.org/10.1093/jxb/erab205
Eremin A, Bulychev AA, Kluge C, Harbinson J, Foissner I (2019) (2019) PH-dependent cell–cell interactions in the green alga Chara. Protoplasma 256:1737–1751. https://doi.org/10.1007/s00709-019-01392-0
doi: 10.1007/s00709-019-01392-0
Evans DE, Williams LE (1998) P-type calcium ATPases in higher plants – biochemical, molecular and functional properties. Biochim Biophys Acta 1376:1–25. https://doi.org/10.1016/s0304-4157(97)00009-9
doi: 10.1016/s0304-4157(97)00009-9
Furch ACU, Hafke JB, Schulz A, van Bel AJE (2007) Ca
doi: 10.1093/jxb/erm143
García-Servín MÁ, Mendoza-Sánchez M, Contreras-Medina LM (2021) Electrical signals as an option of communication with plants: a review. Theor Exp Plant Physiol 33:125–139. https://doi.org/10.1007/s40626-021-00203-3
doi: 10.1007/s40626-021-00203-3
Gerlitz N, Gerum R, Sauer N, Stadler R (2018) Photoinducible DRONPA-s: a new tool for investigating cell–cell connectivity. Plant J 94:751–766. https://doi.org/10.1111/tpj.13918
doi: 10.1111/tpj.13918
Grams TEE, Lautner S, Felle HH et al (2009) Heat-induced electrical signals affect cytoplasmic and apoplastic pH as well as photosynthesis during propagation through the maize leaf. Plant Cell Environ 32:319–326. https://doi.org/10.1111/j.1365-3040.2008.01922.x
doi: 10.1111/j.1365-3040.2008.01922.x
Hedrich R, Neher E (2018) Venus flytrap: how an excitable, carnivorous plant works. Trends Plant Sci 23:220–234. https://doi.org/10.1016/j.tplants.2017.12.004
doi: 10.1016/j.tplants.2017.12.004
Hoepflinger MC, Hoeftberger M, Sommer A, Hametner C, Foissner I (2017) Clathrin in Chara australis: molecular analysis and involvement in charasome degradation and constitutive endocytosis. Front Plant Sci 8:20. https://doi.org/10.3389/fpls.2017.00020
doi: 10.3389/fpls.2017.00020
Johnson CH, Shingles R, Ettinger WF (2007) Regulation and role of calcium fluxes in the chloroplast. In: Wise RR, Hoober JK (eds) The structure and function of plastids. Springer, Dordrecht, pp 403–416. https://doi.org/10.1007/978-1-4020-4061-0_20
Kaňa R, Govindjee (2016) Role of ions in the regulation of light-harvesting. Front Plant Sci 7:1–17. https://doi.org/10.3389/fpls.2016.01849
doi: 10.3389/fpls.2016.01849
Kinoshita T, Nishimura M, Shimazaki K-I (1995) Cytosolic concentration of Ca
doi: 10.1105/tpc.7.8.1333
Koziolek C, Grams TEE, Schreiber U et al (2004) Transient knockout of photosynthesis mediated by electrical signals. New Phytol 161:715–722. https://doi.org/10.1111/j.1469-8137.2004.00985.x
doi: 10.1111/j.1469-8137.2004.00985.x
Kramer DM, Evans JR (2011) The importance of energy balance in improving photosynthetic productivity. Plant Physiol 155:70–78. https://doi.org/10.1104/pp.110.166652
doi: 10.1104/pp.110.166652
Kreimer G, Melkonian M, Latzko E (1985) An electrogenic uniport mediates light-dependent Ca
doi: 10.1016/0014-5793(85)81081-4
Kreimer G, Surek B, Woodrow IE, Latzko E (1987) Calcium binding by spinach stromal proteins. Planta 171:259–265. https://doi.org/10.1007/BF00391103
doi: 10.1007/BF00391103
Król E, Dziubinska H, Trebacz K (2010) What do plants need action potentials for? In: DuBois ML (ed) Action potential: biophysical and cellular context, initiation, phases and propagation. Nova Science, New York, pp 1–26
Krupenina NA, Bulychev AA (2007) Action potential in a plant cell lowers the light requirement for non-photochemical energy-dependent quenching of chlorophyll fluorescence. Biochim Biophys Acta - Bioenerg 1767:781–788. https://doi.org/10.1016/j.bbabio.2007.01.004
doi: 10.1016/j.bbabio.2007.01.004
Krupenina NA, Bulychev AA, Schreiber U (2011) Chlorophyll fluorescence images demonstrate variable pathways in the effects of plasma membrane excitation on electron flow in chloroplasts of Chara cells. Protoplasma 248:513–522. https://doi.org/10.1007/s00709-010-0198-5
doi: 10.1007/s00709-010-0198-5
Lunevsky VZ, Zherelova OM, Vostrikov IY, Berestovsky GN (1983) Excitation of characeae cell membranes as a result of activation of calcium and chloride channels. J Membr Biol 72:43–58. https://doi.org/10.1007/BF01870313
Nikkanen L, Rintamäki E (2019) Chloroplast thioredoxin systems dynamically regulate photosynthesis in plants. Biochem J 476:1159–1172. https://doi.org/10.1042/BCJ20180707
doi: 10.1042/BCJ20180707
Park K, Knoblauch J, Oparka K, Jensen KH (2019) Controlling intercellular flow through mechanosensitive plasmodesmata nanopores. Nat Commun 10:3564. https://doi.org/10.1038/s41467-019-11201-0
doi: 10.1038/s41467-019-11201-0
Pavlovič A, Slováková L, Pandolfi C, Mancuso S (2011) On the mechanism underlying photosynthetic limitation upon trigger hair irritation in the carnivorous plant Venus flytrap (Dionaea muscipula Ellis). J Exp Bot 62:1991–2000. https://doi.org/10.1093/jxb/erq404
doi: 10.1093/jxb/erq404
Pertl-Obermeyer H, Lackner P, Schulze WX et al (2018) Dissecting the subcellular membrane proteome reveals enrichment of H
doi: 10.1371/journal.pone.0201480
Quade BN, Parker MD, Hoepflinger MC, Phipps S, Bisson MA,·Foissner I, Beilby MJ (2021) The molecular identity of the characean OH
Radford JE, Vesk M, Overall RL (1998) Callose deposition at plasmodesmata. Protoplasma 201:30–37. https://doi.org/10.1007/BF01280708
doi: 10.1007/BF01280708
Ruban AV, Johnson MP, Duffy CDP (2012) The photoprotective molecular switch in the photosystem II antenna. Biochim Biophys Acta - Bioenerg 1817:167–181. https://doi.org/10.1016/j.bbabio.2011.04.007
doi: 10.1016/j.bbabio.2011.04.007
Schmölzer PM, Höftberger M, Foissner I (2011) Plasma membrane domains participate in pH banding of Chara internodal cells. Plant Cell Physiol 52:1274–1288. https://doi.org/10.1093/pcp/pcr074
doi: 10.1093/pcp/pcr074
Schürmann P, Buchanan BB (2008) The ferredoxin/thioredoxin system of oxygenic photosynthesis. Antioxid Redox Signal 10:1235–1273. https://doi.org/10.1089/ars.2007.1931
doi: 10.1089/ars.2007.1931
Shimmen T (2007) The sliding theory of cytoplasmic streaming: fifty years of progress. J Plant Res 120:31–43. https://doi.org/10.1007/s10265-006-0061-0
doi: 10.1007/s10265-006-0061-0
Spanswick RM, Costerton JW (1967) Plasmodesmata in Nitella translucens: structure and electrical resistance. J Cell Sci 2:451–464. https://doi.org/10.1242/jcs.2.3.451
doi: 10.1242/jcs.2.3.451
Stonebloom S, Brunkard JO, Cheung AC et al (2012) Redox states of plastids and mitochondria differentially regulate intercellular transport via plasmodesmata. Plant Physiol 158:190–199. https://doi.org/10.1104/pp.111.186130
doi: 10.1104/pp.111.186130
Sukhov V (2016) Electrical signals as mechanism of photosynthesis regulation in plants. Photosynth Res 130:373–387. https://doi.org/10.1007/s11120-016-0270-x
doi: 10.1007/s11120-016-0270-x
Sukhova E, Sukhov V (2021) Electrical signals, plant tolerance to actions of stressors, and programmed cell death: is interaction possible? Plants 10:29–36. https://doi.org/10.3390/plants10081704
doi: 10.3390/plants10081704
Suzuki N, Miller G, Morales J, Shulaev V, Torres MA, Mittler R (2011) Respiratory burst oxidases: the engines of ROS signaling. Curr Opin Plant Biol 14:691–699. https://doi.org/10.1016/j.pbi.2011.07.014
doi: 10.1016/j.pbi.2011.07.014
Tilsner J, Nicolas W, Rosado A, Bayer EM (2016) Staying tight: plasmodesmal membrane contact sites and the control of cell-to-cell connectivity in plants. Annu Rev Plant Biol 67:337–364. https://doi.org/10.1146/annurev-arplant-043015-111840
doi: 10.1146/annurev-arplant-043015-111840
Tsuchiya Y, Yamazaki H, Aoki T (1991) Steady and transient behaviors of protoplasmic streaming in Nitella internodal cell. Biophys J 59:249–251. https://doi.org/10.1016/S0006-3495(91)82215-9
doi: 10.1016/S0006-3495(91)82215-9
Tucker EB, Tucker JE (1993) Cell-to-cell diffusion selectivity in staminal hairs of Setcreasea purpurea. Protoplasma 174:36–44. https://doi.org/10.1007/BF01404040
doi: 10.1007/BF01404040
Vredenberg W, Pavlovič A (2013) Chlorophyll a fluorescence induction (Kautsky curve) in a Venus flytrap (Dionaea muscipula) leaf after mechanical trigger hair irritation. J Plant Physiol 170:242–250. https://doi.org/10.1016/j.jplph.2012.09.009
Wacke M, Thiel G, Hütt MT (2003) Ca
Williamson RE, Ashley CC (1982) Free Ca
doi: 10.1038/296647a0