Analysis of the role of tonoplast H+-ATPase in elongation growth of coleoptile cells of rice seedlings with different growth rates under normoxia and submergence

Anastasia A. Kirpichnikova , Maria O. Biktasheva , Vladislav V. Yemelyanov , Maria F. Shishova

Ecological Genetics ›› 2025, Vol. 23 ›› Issue (1) : 5 -17.

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Ecological Genetics ›› 2025, Vol. 23 ›› Issue (1) : 5 -17. DOI: 10.17816/ecogen641977
Genetic basis of ecosystems evolution
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Analysis of the role of tonoplast H+-ATPase in elongation growth of coleoptile cells of rice seedlings with different growth rates under normoxia and submergence

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Abstract

BACKGROUND: Rice coleoptiles were used to investigate the importance of V H+-ATPase in vacuolization during elongation growth under normoxic and hypoxic conditions.

AIM of the study was to find out a link between growth intensity, protein amount of subunits B and E and transcription of genes encoding those proteins.

MATERIALS AND METHODS: The investigation was carried out on two rice varieties of domestic selection, fast-growing Kuban 3 and slow-growing Amethyst. Seedlings were grown in etiolated conditions at normoxia and submergence. Western-blot analysis was employed to evaluate amount of subunits B and E in microsomal fraction. qRT-PCR was used to distinguish differences in expression of genes encoding subunits B and E of V H+-ATPase.

RESULTS: The growth under aerobic conditions was more consistent with the changes in subunits B and E of V H+-ATPase which was determined at the proteomic level, while the hypoxic growth had a stronger correspondence with changes in OsVHAs gene expression. Varietal differences were revealed only when comparing the transcription intensity, which did not affect the growth dynamics of coleoptiles. Obtained data suggested the existence of differences in the regulation of the enzyme at the transcriptional and proteomic levels during coleoptile elongation.

CONCLUSIONS: The importance of the B and E subunits of V-ATPase involvement in vacuolization during the growth process of rice coleoptiles under different oxygen level was demonstrated.

Keywords

hypoxia / rice Oryza sativa L. / vacuolar H+-ATPase

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Anastasia A. Kirpichnikova, Maria O. Biktasheva, Vladislav V. Yemelyanov, Maria F. Shishova. Analysis of the role of tonoplast H+-ATPase in elongation growth of coleoptile cells of rice seedlings with different growth rates under normoxia and submergence. Ecological Genetics, 2025, 23(1): 5-17 DOI:10.17816/ecogen641977

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References

[1]

Voesenek LACJ, Bailey-Serres J. Flood adaptive traits and processes: An overview. New Phytol. 2015;206(1):57–73. doi: 10.1111/nph.13209

[2]

Voesenek L.A.C.J., Bailey-Serres J. Flood adaptive traits and processes: An overview // New Phytol. 2015. Vol. 206, N 1. P. 57–73. doi: 10.1111/nph.13209

[3]

Bailey-Serres J, Lee SC, Brinton E. Waterproofing crops: Effective flooding survival strategies. Plant Physiol. 2012;160(4):1698–1709. doi: 10.1104/pp.112.208173

[4]

Bailey-Serres J., Lee S.C., Brinton E. Waterproofing crops: Effective flooding survival strategies // Plant Physiol. 2012. Vol. 160, N 4. P. 1698–1709. doi: 10.1104/pp.112.208173

[5]

Ismail AM, Ella ES, Vergara GV, Mackill DJ. Mechanisms associated with tolerance to submergence during germination and early seedling growth in rice (Oryza sativa). Ann Bot. 2009;103(2):197–209. doi: 10.1093/aob/mcn211

[6]

Ismail A.M., Ella E.S., Vergara G.V., Mackill D.J. Mechanisms associated with tolerance to submergence during germination and early seedling growth in rice (Oryza sativa) // Ann Bot. 2009. Vol. 103, N 2. P. 197–209. doi: 10.1093/aob/mcn211

[7]

Su X, Wu H, Xiang J, et al. Evaluation of submergence tolerance of different rice genotypes at seedling emergence stage under water direct seeding. OALibJ. 2022;9(5):e8706. doi: 10.4236/oalib.1108706

[8]

Su X., Wu H., Xiang J., et al. Evaluation of submergence tolerance of different rice genotypes at seedling emergence stage under water direct seeding // OALibJ. 2022. Vol. 9, N 5. ID e8706. doi: 10.4236/oalib.1108706

[9]

Bogdanova EM, Bertova AD, Kirpichnikova AA, et al. Growth and viability of coleoptiles under oxygen deficiency in Oryza sativa L. From the collection of the federal rice research center. Agricultural Biology. 2023;58(3):538–553. doi: 10.15389/agrobiology.2023.3.538rus EDN: XOZZKM

[10]

Богданова Е.М., Бертова А.Д., Кирпичникова А.А., и др. Показатели роста и устойчивости к дефициту кислорода у колеоптилей Oryza sativa L. из коллекции Федерального научного центра риса // Сельскохозяйственная биология. 2023. Т. 58, № 3. С. 538–553. doi: 10.15389/agrobiology.2023.3.538rus EDN: XOZZKM

[11]

Kirpichnikova AA, Kudoyarova GR, Yemelyanov VV, Shishova MF. The peculiarities of cell elongation growth of cereal coleoptiles under normal and flooding conditions. Ecological genetics. 2023;21(4): 401–417. doi: 10.17816/ecogen623901 EDN: QWDPWQ

[12]

Кирпичникова А.А., Кудоярова Г.Р., Емельянов В.В., Шишова М.Ф. Особенности роста растяжением клеток колеоптилей злаков в норме и при затоплении // Экологическая генетика. 2023. Т. 21, № 4. С. 401–417. doi: 10.17816/ecogen623901 EDN: QWDPWQ

[13]

O’Sullivan PA, Weiss GM, Friesen D. Tolerance of spring wheat (Triticum aestivum L.) to trifluralin deep-incorporated in the autumn or spring. Weed Res. 1985;25(4):275–280. doi: 10.1111/j.1365-3180.1985.tb00645.x

[14]

O’Sullivan P.A., Weiss G.M., Friesen D. Tolerance of spring wheat (Triticum aestivum L.) to trifluralin deep-incorporated in the autumn or spring // Weed Res. 1985. Vol. 25, N 4. P. 275–280. doi: 10.1111/j.1365-3180.1985.tb00645.x

[15]

Brown PR, Singleton GR, Tann CR, Mock I. Increasing sowing depth to reduce mouse damage to winter crops. Crop Prot. 2003;22(4):653–660. doi: 10.1016/S0261-2194(03)00006-1

[16]

Brown P.R., Singleton G.R., Tann C.R., Mock I. Increasing sowing depth to reduce mouse damage to winter crops // Crop Prot. 2003. Vol. 22, N 4. P. 653–660. doi: 10.1016/S0261-2194(03)00006-1

[17]

Rebetzke GJ, Zheng B, Chapman SC. Do wheat breeders have suitable genetic variation to overcome short coleoptiles and poor establishment in the warmer soils of future climates? Funct Plant Biol. 2016;43(10):961–972. doi: 10.1071/FP15362

[18]

Rebetzke G.J., Zheng B., Chapman S.C. Do wheat breeders have suitable genetic variation to overcome short coleoptiles and poor establishment in the warmer soils of future climates? // Funct Plant Biol. 2016. Vol. 43, N 10. P. 961–972. doi: 10.1071/FP15362

[19]

Kordan HA. Patterns of shoot and root growth in rice seedlings germinating under water. J Appl Ecol. 1974;11(2):685–690. doi: 10.2307/2402218

[20]

Kordan H.A. Patterns of shoot and root growth in rice seedlings germinating under water // J Appl Ecol. 1974. Vol. 11, N 2. P. 685–690. doi: 10.2307/2402218

[21]

Shiono K, Koshide A, Iwasaki K, et al. Imaging the snorkel effect during submerged germination in rice: Oxygen supply via the coleoptile triggers seminal root emergence underwater. Front Plant Sci. 2022;13:946776. doi: 10.3389/fpls.2022.946776

[22]

Shiono K., Koshide A., Iwasaki K., et al. Imaging the snorkel effect during submerged germination in rice: Oxygen supply via the coleoptile triggers seminal root emergence underwater // Front Plant Sci. 2022. Vol. 13. ID 946776. doi: 10.3389/fpls.2022.946776

[23]

Arsuffi G, Braybrook SA. Acid growth: an ongoing trip. J Exp Bot. 2018;69(2):137–146. doi: 10.1093/jxb/erx390

[24]

Arsuffi G., Braybrook S.A. Acid growth: an ongoing trip // J Exp Bot. 2018. Vol. 69, N 2. P. 137–146. doi: 10.1093/jxb/erx390

[25]

Kirpichnikova А, Chen Т, Teplyakova S, Shishova M. Proton pump and plant cell elongation. Biol Commun. 2018;63(1):32–42. doi: 10.21638/spbu03.2018.105

[26]

Kirpichnikova А., Chen Т., Teplyakova S., Shishova M. Proton pump and plant cell elongation // Biol Commun. 2018. Vol. 63, N 1. P. 32–42. doi: 10.21638/spbu03.2018.105

[27]

Merzendorfer H, Graf R, Huss M, et al. Regulation of proton translocating V-ATPases. J Exp Biol. 1997;200(2):225–235. doi: 10.1242/jeb.200.2.225

[28]

Merzendorfer H., Graf R., Huss M., et al. Regulation of proton translocating V-ATPases // J Exp Biol. 1997. Vol. 200, N 2. P. 225–235. doi: 10.1242/jeb.200.2.225

[29]

Dettmer J, Hong-Hermesdorf A, Stierhof Y-D, Schumacher K. Vacuolar H+-ATPase activity is regulated for endocytic and secretory trafficking in Arabidopsis. Plant Cell. 2006;18(3):715–730. doi: 10.1105/tpc.105.037978

[30]

Dettmer J., Hong-Hermesdorf A., Stierhof Y.-D., Schumacher K. Vacuolar H+-ATPase activity is regulated for endocytic and secretory trafficking in Arabidopsis // Plant Cell. 2006. Vol. 18, N 3. P. 715–730. doi: 10.1105/tpc.105.037978

[31]

Seidel T. The plant V-ATPase. Front Plant Sci. 2022;13:931777. doi: 10.3389/fpls.2022.931777

[32]

Seidel T. The plant V-ATPase // Front Plant Sci. 2022. Vol. 13. ID 931777. doi: 10.3389/fpls.2022.931777

[33]

Kirpichnikova АА, Chen Т, Romanyuk DА, et al. Peculiar features of plant cell vacuolar H+-ATPase regulation. Biological Communications. 2016;(2):149–160. doi: 10.21638/11701/spbu03.2016.212 EDN: WIQTGD

[34]

Кирпичникова А.А., Чэнь Т., Романюк Д.А., и др. Особенности регуляции вакуолярной Н+-АТФазы растительных клеток // Вестник Санкт-Петербургского университета. Сер. 3. Биология. 2016. № 2. С. 149–160. doi: 10.21638/11701/spbu03.2016.212 EDN: WIQTGD

[35]

Yemelyanov VV, Lastochkin VV, Chirkova TV, et al. Indoleacetic acid levels in wheat and rice seedlings under oxygen deficiency and subsequent reoxygenation. Biomolecules. 2020;10(2):276. doi: 10.3390/biom10020276

[36]

Yemelyanov V.V., Lastochkin V.V., Chirkova T.V., et al. Indoleacetic acid levels in wheat and rice seedlings under oxygen deficiency and subsequent reoxygenation // Biomolecules. 2020. Vol. 10, N 2. ID 276. doi: 10.3390/biom10020276

[37]

Shishova MF, Tankelyun OV, Rudashevskaya EL, et al. Alteration of transport activity of proton pumps in coleoptile cells during early development stages of maize seedlings. Russian Journal of Developmental Biology. 2012;43(6):413–424. EDN: PDDSEV

[38]

Шишова М.Ф., Танкелюн О.В., Рудашевская Е.Л., и др. Изменение транспортной активности протонных насосов клеток колеоптилей на ранних этапах развития проростков кукурузы // Онтогенез. 2012. Т. 43, № 6. С. 413–424. EDN: PDDSEV

[39]

Laemmli UK. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970;227(5259):680–683. doi: 10.1038/227680a0

[40]

Laemmli U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4 // Nature. 1970. Vol. 227, N 5259. P. 680–683. doi: 10.1038/227680a0

[41]

Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976;72(1–2):248–254. doi: 10.1016/0003-2697(76)90527-3

[42]

Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding // Anal Biochem. 1976. Vol. 72, N 1–2. P. 248–254. doi: 10.1016/0003-2697(76)90527-3

[43]

Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2–ΔΔCT method. Methods. 2001;25(4):402–408. doi: 10.1006/meth.2001.1262

[44]

Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2–ΔΔCT method // Methods. 2001. Vol. 25, N 4. P. 402–408. doi: 10.1006/meth.2001.1262

[45]

Schumacher K, Krebs M. The V-ATPase: Small cargo, large effects. Curr Opin Plant Biol. 2010;13(6):724–730. doi: 10.1016/j.pbi.2010.07.003

[46]

Schumacher K., Krebs M. The V-ATPase: Small cargo, large effects // Curr Opin Plant Biol. 2010. Vol. 13, N 6. P. 724–730. doi: 10.1016/j.pbi.2010.07.003

[47]

Wang C, Xiang Y, Qian D. Current progress in plant V-ATPase: From biochemical properties to physiological functions. J Plant Physiol. 2021;266:153525. doi: 10.1016/j.jplph.2021.153525

[48]

Wang C., Xiang Y., Qian D. Current progress in plant V-ATPase: From biochemical properties to physiological functions // J Plant Physiol. 2021. Vol. 266. ID 153525. doi: 10.1016/j.jplph.2021.153525

[49]

Raghavendra AS, Ye W, Kinoshita T. Editorial: pH as a signal and secondary messenger in plant cells. Front Plant Science. 2023;14:1148689. doi: 10.3389/fpls.2023.1148689

[50]

Raghavendra A.S., Ye W., Kinoshita T. Editorial: pH as a signal and secondary messenger in plant cells // Front Plant Science. 2023. Vol. 14. ID 1148689. doi: 10.3389/fpls.2023.1148689

[51]

Felle HH. pH: Signal and messenger in plant cells. Plant Biol. 2001;3(6):577–591. doi: 10.1055/s-2001-19372

[52]

Felle H.H. pH: Signal and messenger in plant cells // Plant Biol. 2001. Vol. 3, N 6. P. 577–591. doi: 10.1055/s-2001-19372

[53]

Felle HH. pH regulation in anoxic plants. Ann Bot. 2005;96(4): 519–532. doi: 10.1093/aob/mci207

[54]

Felle H.H. pH regulation in anoxic plants // Ann Bot. 2005. Vol. 96, N 4. P. 519–532. doi: 10.1093/aob/mci207

[55]

Drew MC. Oxygen deficiency and root metabolism: Injury and acclimation under hypoxia and anoxia. Annu Rev Plant Physiol Plant Mol Biol. 1997;48:223–250. doi: 10.1146/annurev.arplant.48.1.223

[56]

Drew M.C. Oxygen deficiency and root metabolism: Injury and acclimation under hypoxia and anoxia // Annu Rev Plant Physiol Plant Mol Biol. 1997. Vol. 48. P. 223–250. doi: 10.1146/annurev.arplant.48.1.223

[57]

Chirkova T, Yemelyanov V. The study of plant adaptation to oxygen deficiency in Saint Petersburg University. Biol Commun. 2018;63(1):17–31. doi: 10.21638/spbu03.2018.104

[58]

Chirkova T., Yemelyanov V. The study of plant adaptation to oxygen deficiency in Saint Petersburg University // Biol Commun. 2018. Vol. 63, N 1. P. 17–31. doi: 10.21638/spbu03.2018.104

[59]

Kulichikhin KY, Aitio O, Chirkova TV, Fagerstedt KV. Effect of oxygen concentration on intracellular pH, glucose-6-phosphate and NTP content in rice (Oryza sativa) and wheat (Triticum aestivum) root tips: In vivo 31P-NMR study. Physiol Plant. 2007;129(3):507–518. doi: 10.1111/j.1399-3054.2006.00819.x

[60]

Kulichikhin K.Y., Aitio O., Chirkova T.V., Fagerstedt K.V. Effect of oxygen concentration on intracellular pH, glucose-6-phosphate and NTP content in rice (Oryza sativa) and wheat (Triticum aestivum) root tips: In vivo 31P-NMR study // Physiol Plant. 2007. Vol. 129, N 3. P. 507–518. doi: 10.1111/j.1399-3054.2006.00819.x

[61]

Yemelyanov VV, Chirkova TV, Lindberg SM, Shishova MF. Potassium efflux and cytosol acidification as primary anoxia-induced events in wheat and rice seedlings. Plants. 2020;9(9):1216. doi: 10.3390/plants9091216

[62]

Yemelyanov V.V., Chirkova T.V., Lindberg S.M., Shishova M.F. Potassium efflux and cytosol acidification as primary anoxia-induced events in wheat and rice seedlings // Plants. 2020. Vol. 9, N 9. ID 1216. doi: 10.3390/plants9091216

[63]

Greenway H, Kulichikhin KY, Cawthray GR, Colmer TD. pH regulation in anoxic rice coleoptiles at pH 3.5: Biochemical pH-stats and net H+ influx in the absence and presence of NOFormula. J Exp Bot. 2012;63(5):1969–1983. doi: 10.1093/jxb/err395

[64]

Greenway H., Kulichikhin K.Y., Cawthray G.R., Colmer T.D. pH regulation in anoxic rice coleoptiles at pH 3.5: Biochemical pH-stats and net H+ influx in the absence and presence of NOFormula // J Exp Bot. 2012. Vol. 63, N 5. P. 1969–1983. doi: 10.1093/jxb/err395

[65]

Narsai R, Secco D, Schultz MD, et al. Dynamic and rapid changes in the transcriptome and epigenome during germination and in developing rice (Oryza sativa) coleoptiles under anoxia and re-oxygenation. Plant J. 2017;89(4):805–824. doi: 10.1111/tpj.13418

[66]

Narsai R., Secco D., Schultz M.D., et al. Dynamic and rapid changes in the transcriptome and epigenome during germination and in developing rice (Oryza sativa) coleoptiles under anoxia and re-oxygenation // Plant J. 2017. Vol. 89, N 4. P. 805–824. doi: 10.1111/tpj.13418

[67]

Nghi KN, Tondelli A, Valè G, et al. Dissection of coleoptile elongation in japonica rice under submergence through integrated genome-wide association mapping and transcriptional analyses. Plant Cell Environ. 2019;42(6):1832–1846. doi: 10.1111/pce.13540

[68]

Nghi K.N., Tondelli A., Valè G., et al. Dissection of coleoptile elongation in japonica rice under submergence through integrated genome-wide association mapping and transcriptional analyses // Plant Cell Environ. 2019. Vol. 42, N 6. P. 1832–1846. doi: 10.1111/pce.13540

[69]

Pucciariello C. Molecular mechanisms supporting rice germination and coleoptile elongation under low oxygen. Plants. 2020;9(8):1037. doi: 10.3390/plants9081037

[70]

Pucciariello C. Molecular mechanisms supporting rice germination and coleoptile elongation under low oxygen // Plants. 2020. Vol. 9, N 8. ID 1037. doi: 10.3390/plants9081037

[71]

Gruber G, Wieczorek H, Harvey WR, Muller V. Structure-function relationship of A-, F- and V-ATPases. J Exp Biol. 2001;204(15): 2597–2605. doi: 10.1242/jeb.204.15.2597

[72]

Gruber G., Wieczorek H., Harvey W.R., Muller V. Structure-function relationship of A-, F- and V-ATPases // J Exp Biol. 2001. Vol. 204, N 15. P. 2597–2605. doi: 10.1242/jeb.204.15.2597

[73]

Sze H, Schumacher K, Muller ML, et al. A simple nomenclature for a complex proton pump: VHA genes encode the vacuolar H+-ATPase. Trends Plant Sci. 2002;7(4):157–161. doi: 10.1016/s1360-1385(02)02240-9

[74]

Sze H., Schumacher K., Muller M.L., et al. A simple nomenclature for a complex proton pump: VHA genes encode the vacuolar H+-ATPase // Trends Plant Sci. 2002. Vol. 7, N 4. P. 157–161. doi: 10.1016/s1360-1385(02)02240-9

[75]

Dettmer J, Schubert D, Calvo-Weimar O, et al. Essential role of the V-ATPase in male gametophyte development. Plant J. 2005;41(1):117–124. doi: 10.1111/j.1365-313X.2004.02282.x

[76]

Dettmer J., Schubert D., Calvo-Weimar O., et al. Essential role of the V-ATPase in male gametophyte development // Plant J. 2005. Vol. 41, N 1. P. 117–124. doi: 10.1111/j.1365-313X.2004.02282.x

[77]

Dettmer J, Liu T-Y, Schumacher K. Functional analysis of Arabidopsis V-ATPase subunit VHA-E isoforms. Eur J Cell Biol. 2010;89(2–3): 152–156. doi: 10.1016/j.ejcb.2009.11.008

[78]

Dettmer J., Liu T.-Y., Schumacher K. Functional analysis of Arabidopsis V-ATPase subunit VHA-E isoforms // Eur J Cell Biol. 2010. Vol. 89, N 2–3. P. 152–156. doi: 10.1016/j.ejcb.2009.11.008

[79]

Chen S-H, Bubb MR, Yarmola EG, et al. Vacuolar H+-ATPase binding to microfilaments: regulation in response to phosphatidylinositol 3-kinase activity and detailed characterization of the actin-binding site in subunit B. J Biol Chem. 2004;279(9):7988–7998. doi: 10.1074/jbc.M305351200

[80]

Chen S.-H., Bubb M.R., Yarmola E.G., et al. Vacuolar H+-ATPase binding to microfilaments: regulation in response to phosphatidylinositol 3-kinase activity and detailed characterization of the actin-binding site in subunit B // J Biol Chem. 2004. Vol. 279, N 9. P. 7988–7998. doi: 10.1074/jbc.M305351200

[81]

Lu M, Ammar D, Ives H, et al. Physical interaction between aldolase and vacuolar H+-ATPase is essential for the assembly and activity of the proton pump. J Biol Chem. 2007;282(34):24495–24503. doi: 10.1074/jbc.M702598200

[82]

Lu M., Ammar D., Ives H., et al. Physical interaction between aldolase and vacuolar H+-ATPase is essential for the assembly and activity of the proton pump // J Biol Chem. 2007. Vol. 282, N 34. P. 24495–24503. doi: 10.1074/jbc.M702598200

[83]

Wang L, He X, Zhao Y, et al. Wheat vacuolar H+-ATPase subunit B cloning and its involvement in salt tolerance. Planta. 2011;234(1):1–7. doi: 10.1007/s00425-011-1383-2

[84]

Wang L., He X., Zhao Y., et al. Wheat vacuolar H+-ATPase subunit B cloning and its involvement in salt tolerance // Planta. 2011. Vol. 234, N 1. P. 1–7. doi: 10.1007/s00425-011-1383-2

[85]

Hanitzsch M, Schnitzer D, Seidel T, et al. Transcript level regulation of the vacuolar H+-ATPase subunit isoforms VHA-А, VHA-E and VHA-G in Arabidopsis thaliana. Mol Membr Biol. 2007;24 (5–6):507–518. doi: 10.1080/09687680701447393

[86]

Hanitzsch M., Schnitzer D., Seidel T., et al. Transcript level regulation of the vacuolar H+-ATPase subunit isoforms VHA-А, VHA-E and VHA-G in Arabidopsis thaliana // Mol Membr Biol. 2007. Vol. 24, N 5–6. P. 507–518. doi: 10.1080/09687680701447393

[87]

Löw R, Rockel B, Kirsch M, et al. Early salt stress effects on the differential expression of vacuolar H+-ATPase genes in roots and leaves of Mesembryanthemum crystallinum. Plant Physiol. 1996;110(1):259–265. doi: 10.1104/pp.110.1.259

[88]

Löw R., Rockel B., Kirsch M., et al. Early salt stress effects on the differential expression of vacuolar H+-ATPase genes in roots and leaves of Mesembryanthemum crystallinum // Plant Physiol. 1996. Vol. 110, N 1. P. 259–265. doi: 10.1104/pp.110.1.259

[89]

Golldack D, Dietz K-J. Salt-induced expression of the vacuolar H+-ATPase in the common ice plant is developmentally controlled and tissue specific. Plant Physiol. 2001;125(4):1643–1654. doi: 10.1104/pp.125.4.1643

[90]

Golldack D., Dietz K.-J. Salt-induced expression of the vacuolar H+-ATPase in the common ice plant is developmentally controlled and tissue specific // Plant Physiol. 2001. Vol. 125, N 4. P. 1643–1654. doi: 10.1104/pp.125.4.1643

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