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Activation and activity of plasma membrane H+-ATPase: key events in germinating Vicia faba seeds

Published online by Cambridge University Press:  06 May 2021

N.V. Obroucheva*
Affiliation:
Institute of Plant Physiology, Russian Academy of Sciences, Botanicheskaya ul. 35, Moscow127276, Russia
S.V. Lityagina
Affiliation:
Institute of Plant Physiology, Russian Academy of Sciences, Botanicheskaya ul. 35, Moscow127276, Russia
I.A. Sinkevich
Affiliation:
Institute of Plant Physiology, Russian Academy of Sciences, Botanicheskaya ul. 35, Moscow127276, Russia
*
*Author of Correspondence: N.V. Obroucheva, E-mail: [email protected]

Abstract

The regulation of plasma membrane H+-ATPase was considered in imbibing Vicia faba seeds, a distinctive feature of which is germination by cell elongation, whereas the mitotic activity starts later. The enzyme activation is known to precede germination because it provides H+ ion efflux from the cytoplasm to cell walls which favours their modification and loosening, being the prerequisites of cell elongation commencement. The presence of an enzyme in imbibing embryo axes was confirmed immunochemically. H+ ion efflux was recorded with a pH-meter as acidification of ambient solution by the embryonic axes for 5 min. The activation of the enzyme and its subsequent activity are regulated in different ways. Enzyme activation is hydration-driven, it starts when water content increases up to the threshold level of 55% (fresh weight basis). This value was confirmed by imbibition in the presence of the osmoticum polyethylene glycol 6000, at various osmotic potentials. The activation does not depend on indolylacetic or abscisic acid treatment. Hydration-triggered activation of the enzyme favours rapid seed germination and its correspondence to the soil water potential. Enzyme activity after its activation is inhibited by 60–70% by 10−5–10−7 M abscisic acid, whereas indolylacetic acid exerted no effect. The regulation of plasma membrane H+-ATPase activity is presumably accomplished by the interaction of the enzyme with 14-3-3 proteins and endogenous fusicoccin, present in imbibing axes.

Type
Research Paper
Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press

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References

Antipova, OV, Bartova, LM, Kalashnikova, TS, Obroucheva, NV, Voblikova, VD and Muromtsev, GS (2003) Fusicoccin-induced cell elongation and endogenous fusicoccin-like ligands in germinating seeds. Plant Physiology and Biochemistry 41, 157164.CrossRefGoogle Scholar
Arsuffi, G and Braybrook, SA (2018) Acid growth: an ongoing trip. Journal of Experimental Botany 69, 137146.CrossRefGoogle ScholarPubMed
Borch, J, Bych, K, Roepstorff, A, Palmgren, MG and Fuglsang, AT (2002) Phosphorylation-independent interaction between 14-3-3 protein and plasma membrane H+-ATPase. Biochemical Society Transactions 30, 411415.CrossRefGoogle ScholarPubMed
Buch-Pedersen, MJ and Palmgren, MG (2003) Mechanism of proton transport by plant plasma membrane. Journal of Plant Research 116, 507515.CrossRefGoogle ScholarPubMed
Buch-Pedersen, MJ, Pedersen, BP, Veierskov, B, Nissen, P and Palmgren, MG (2009) Protons and how they are transported by proton pumps. European Journal of Physiology 457, 573579.CrossRefGoogle ScholarPubMed
Camoni, L, Visconti, S and Aducci, P (2013) The phytotoxin fusicoccin, a selective stabilizer of 14-3-3 interactions. JUBMB Life 65, 513517.CrossRefGoogle ScholarPubMed
De Bont, L, Naim, E, Arbelet-Bonnin, D, Xia, Q, Palm, E, Meimoun, P, Mancuso, S, El-Maarouf-Bouteau, H and Bouteau, F (2019) Activation of plasma membrane H+-ATPases participates in dormancy alleviation in sunflower seeds. Plant Science 280, 408415.CrossRefGoogle ScholarPubMed
Falhof, J, Petersen, JT, Fuglsang, AT and Palmgren, M (2016) Plasma membrane H+-ATPase regulation in the center of plant physiology. Molecular Plant 9, 323337.CrossRefGoogle Scholar
Fuglsang, AT, Borch, J, Bych, K, Jahn, TC and Roepstorff, P (2003) The binding site for regulatory 14-3-3 protein in plasma membrane H+-ATPase – involvement of a region promoting phosphorylation-independent interaction in addition to the phosphorylation-dependent C-terminal end. Journal of Biological Chemistry 278, 4226642272.CrossRefGoogle ScholarPubMed
Galland, M, Huguot, R, Arc, E, Cueff, G, Job, D and Rajjou, L (2014) Dynamic proteomics emphasizes the importance of selective mRNA translation and protein turnover during Arabidopsis seed germination. Моlecular Cellular Proteomics 13, 252268.CrossRefGoogle ScholarPubMed
Guerra, F and Bondar, A-N (2015) Dynamics of the plasma membrane proton pump. Journal of Membrane Biology 248, 443453.CrossRefGoogle ScholarPubMed
Hager, A (2003) Role of the plasma membrane H+-ATPase in auxin-induced elongation growth: historical and new aspects. Journal of Plant Research 116, 483505.CrossRefGoogle ScholarPubMed
Harper, JF, Manney, L and Sussman, MR (1994) The plasma-membrane H+-gene family in Arabidopsis: genomic sequence of AHA10 which is expressed primarily in developing seeds. Molecular Genetics and Genomics 244, 572587.CrossRefGoogle Scholar
Hayashi, Y, Takahashi, K, Inoue, S and Kinoshita, T (2014) Abscisic acid suppresses hypocotyl elongation by dephosphorylating plasma membrane H+-ATPase in Arabidopsis thaliana. Plant & Cell Physiology 55, 845853.CrossRefGoogle ScholarPubMed
Janicka-Russak, M, Kabala, K, Wdowikowska, A and Klobus, G (2012) Response of plasma membrane H+-ATPase to low temperature in cucumber roots. Journal of Plant Research 125, 291300.CrossRefGoogle ScholarPubMed
Kimura, M and Nambara, E (2010) Stored and neosynthesized mRNA in Arabidopsis seeds: effects of cycloheximide and controlled deterioration treatment on the resumption of transcription during imbibition. Plant Molecular Biology 73, 119129.CrossRefGoogle ScholarPubMed
Obroucheva, NV, Lityagina, SV and Sinkevich, IA (2018) Plasma membrane H+-ATPase during embryo dormancy and dormancy release in horse chestnut seeds. International Journal of Cell Science and Molecular Biology 4(3) doi:10.19080/IJCSMB.2018.04.555639Google Scholar
Obroucheva, N, Sinkevich, I and Lityagina, S (2016) Physiological aspects of seed recalcitrance: a case study on the tree Aesculus hippocastanum. Tree Physiology 36, 11271150.CrossRefGoogle ScholarPubMed
Obroucheva, NV (2012) Transition from hormonal to nonhormonal regulation as exemplified by seed dormancy release and germination triggering. Russian Journal of Plant Physiology 59, 546555.CrossRefGoogle Scholar
Obroucheva, NV (2017) Participation of plasma membrane H+-ATPase in seed germination. International Journal of Cell Science and Molecular Biology 2(3). doi:10.19080/IJCSMB.2017.02.555589Google Scholar
Obroucheva, NV, Sinkevich, IA, Lityagina, SV and Novikova, GV (2013) Activation of acid growth in germinating horse chestnut seeds. Russian Journal of Plant Physiology 60, 437441.CrossRefGoogle Scholar
Park, YB and Cosgrove, DJ (2015) Xyloglucan and its interactions with other components of the growing cell wall. Plant & Cell Physiology 56, 180194.CrossRefGoogle ScholarPubMed
Planes, MD, Ninoles, R, Rubio, L, Rissoli, G, Rueso, E, Garcia-Sanchez, M-J, Alejandro, S, Gonzales-Guzman, M, Hedrich, R, Rodriguez, PL, Fernandez, JA and Serrano, R (2015) A mechanism of growth inhibition by abscisic acid in germinating seeds of Arabidopsis thaliana based on inhibition of plasma membrane H+-ATPase and decreased cytosolic pH, K+, and anions. Journal of Experimental Botany 66, 813825.CrossRefGoogle ScholarPubMed
Pless, T, Böttger, M, Hedden, P and Graebe, J (1984) Occurrence of 4-Cl-indoleacetic acid in broad beans and correlation of its level with seed development. Plant Physiology 74, 320323.CrossRefGoogle Scholar
Portillo, F (2000) Regulation of plasma membrane H(+)-ATPase in fungi and plants. Biochimica et Biophysica Acta 1469, 3142.CrossRefGoogle ScholarPubMed
Rober-Kleber, N, Albrechtova, JT, Fleig, S, Huck, N, Michalke, W, Wagner, E, Speth, V, Neuhaus, G and Fischer-Iglesias, C (2003) Plasma membrane H+-ATPase is involved in auxin-mediated cell elongation during wheat embryo development. Plant Physiology 131, 13021312.CrossRefGoogle ScholarPubMed
Rudashevskaya, E, Kirpichnikova, A and Shishova, M (2005) Activity of H+-ATPase in coleoptile plasma membrane within maize seedling development. Russian Journal of Plant Physiology 52, 239245.CrossRefGoogle Scholar
Sanchez-Nieto, SS, Enriquez-Arredondo, C, Guzman-Chavez, F, Hernandez-Murioz, R, Ramirez, J and Gavilanes-Ruiz, M (2011) Kinetics of the H+-ATPase from dry and 5-hours imbibed reconstituted forms. Molecular Plant 4, 505515.CrossRefGoogle ScholarPubMed
Sztein, AE, Ilic, N, Cohen, JD and Cooke, TJ (2002) Indole-3-acetic acid biosynthesis in isolated axes from germinating bean seeds: the effect of wounding on the biosynthetic pathway. Plant Growth Regulation 36, 201207.CrossRefGoogle Scholar
Takahashi, K, Hayashi, K and Kinoshita, T (2012) Auxin activates the plasma membrane H+-ATPase by phosphorylation during hypocotyl elongation in Arabidopsis. Journal of Plant Physiology 159, 632641.CrossRefGoogle ScholarPubMed
Towbin, H, Staehelin, T and Gordon, J (1979) Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proceedings of the National Academy of Sciences of the United States of America 76, 43504354.CrossRefGoogle ScholarPubMed