Експресія аквапорину PIP2;1 як ознака посухостійкості гібридів Zea mays L. за умов зниженої вологості ґрунту

Г. В. Шевченко; І. І. Овруцька; Ю. В. Овчаренко

doi:10.21498/2518-1017.15.2.2019.173572

Authors

Г. В. Шевченко Institute of Botany, NAS of Ukraine, Ukraine https://orcid.org/0000-0001-5826-025X
І. І. Овруцька Institute of Botany, NAS of Ukraine, Ukraine https://orcid.org/0000-0002-5829-1424
Ю. В. Овчаренко Institute of Botany, NAS of Ukraine, Ukraine https://orcid.org/0000-0002-5527-504X

DOI:

https://doi.org/10.21498/2518-1017.15.2.2019.173572

Keywords:

corn, aquaporin PIP2, 1, sterols, phospholipids, unsaturated fatty acids, roots, water deficiency, drought tolerance

Abstract

Purpose. To investigate expression of aquaporin PIP2;1 in maize cultivars ‘Pereiaslavskyi’ and ‘Dostatok’, (moderately drought-resistant) and ‘Yachta’ and ‘Flahman’ (drought-resistant), which grew for 10 days in low humidity substrate (30%). To evaluate possible influence of lipids and fatty acids on the functional activity of PIP2;1 under above humidity conditions.

Methods. Biochemical: study of lipids and fatty acids in cytoplasmic membrane fraction from the roots (liquid chromatography); molecular: detection of the relative expression of aquaporin PIP2;1 in the roots (polymerase chain reaction, PCR); morphometric measurements and statistical methods for result processing.

Results. Studies showed that in moderately drought-tolerant maize cultivars ‘Pereiaslavskyi’ and ‘Yachta’, PIP2;1 expression decreased, while in drought-tolerant ‘Dostatok’ and ‘Flahman’, on the contrary, it increased. In ‘Dostatok’ and ‘Flahman’ smaller root water deficit compared with ‘Pereiaslavskyi’ and ‘Yachta’ in conditions of low humidity of the substrate was recorded. In addition, the quantity of sterols and phospholipids increased in the plasma membrane of all hybrids.

Conclusions. Reduced expression of PIP2;1 observed in ‘Pereiaslavskyi’ and ‘Yachta’, is a characteristic feature of not drought tolerant plants and indicates reaction to a decrease in substrate moisture and counteraction to dehydration, since a smaller amount of aquaporins ensures water retention in the cells. Contrary, at a substrate moisture content of 30%, PIP2;1 expression in drought-resistant hybrids ‘Dostatok’ and ‘Flahman’ increased which was accompanied by lesser root water deficiency (comparing to that of ‘Pereiaslavskyi’ and ‘Yachta’). It is quite probable that the enhanced expression of the PIP2;1 isoform in cultivars ‘Dostatok’ and ‘Flahman’ is a specific indicator of hybrids drought resistance. The obtained data are important for improving the selection of drought resistant maize hybrids.

Downloads

Download data is not yet available.

Author Biographies

Г. В. Шевченко, Institute of Botany, NAS of Ukraine

Shevchenko, H. V.

І. І. Овруцька, Institute of Botany, NAS of Ukraine

Ovrutska, I. I.

Ю. В. Овчаренко, Institute of Botany, NAS of Ukraine

Ovcharenko, Yu. V.

References

Gronnier, J., Crowet, J.-M., Habenstein, B., Nasir, M. N., Bayle, V., Hosy, E., … Mongrand, S. (2017). Structural basis for plant plasma membrane protein dynamics and organization into functional nanodomains. eLife, 6, e26404. doi: 10.7554/eLife.26404

Luu, D. T., & Maurel, C. (2005). Aquaporins in a challenging environment: molecular gears for adjusting plant water status. Plant Cell Envir., 28(1), 85–96. doi: 10.1111/j.1365-3040.2004.01295.x

Reizer, J., Reizer, A., & Saier, M. (1993). The МІР family of integral membrane channel proteins: sequence comparisons, evolutionary relationships, reconstructed pathway of evolution, and proposed functional differentiation of the two repeated halves of the proteins. Crit. Rev. Biochem. Моl. Biol., 28(3), 235–257. doi: 10.3109/10409239309086796

Maurel, C., Verdoucq, L., Luu, D. T., & Santoni, V. (2008). Plant aquaporins: membrane channels with multiple integrated functions. Annu. Rev. Plant Biol., 59(1), 595–624. doi: 10.1146/annurev.arplant.59.032607.092734

Chaumont, F., & Tyerman, S. D. (2014). Aquaporins: highly regulated channels controlling plant water relations. Plant Physiol., 164(4), 1600–1618. doi: 10.1104/pp.113.233791

Chaumont, F., Barrieu, F., Wojcik, E., Chrispeels, M. J., & Jung, R. (2001). Aquaporins constitute a large and highly divergent protein family in maize. Plant Physiol., 125(3), 1206–1215. doi: 10.1104/pp.125.3.1206

Chaumont, F., Barrieu, F., Jung, R., & Chrispeels, M. (2000). Plasma membrane intrinsic proteins from maize cluster in two sequence subgroups with differential aquaporin activity. Plant Physiol., 122(4), 1025–1034. doi: 10.1104/pp.122.4.1025

Mahdieh, M., Mostajeran, A., Horie, N., & Katsuhara, M. (2008). Drought stress alters water relations and expression of PIP-type aquaporin genes in Nicotiana tabacum plants. Plant Cell Physiol., 49(5), 801–813. doi: 10.1093/pcp/pcn054

Voitsekhivska, O. V., Kapustian, A. V., Kosyk, O. I., Musiienko, M. M., Olkhovych, O. P., Paniuta, O. O., Parshykova, T. V., & Slavny, P. S. (2010). Fiziolohiia roslyn. Praktykum [Plant Physiology. Workshop] (pp. 75–77). T. V. Parshykova (Ed.). Lutsk: Teren. [in Ukrainian]

Larsson, C., Sommarin, M., & Widell, S. (1994). Isolation of highly purified plant plasma membranes and separation of inside-out and right-side-out vesicles. Methods Enzymol., 228, 451–469. doi: 10.1016/00766879(94)28046-0

Carde, J.-P. (1987). Electron microscopy of plant cell membranes. Methods Enzymol., 148, 599–622. doi: 10.1016/0076-6879(87)48058-0

Chen, S.-H. S., & Kou, A. Y. (1982). Improved procedure for the separation of phospholipids by high-performance liquid chromatography. J. Chromatogr. B Biomed. Sci. Appl., 227(1), 25–31. doi: 10.1016/S0378-4347(00)80352-7

Subbarao, G. V., Nam, N. H., Chauhan, Y. S., & Johansen, C. (2000). Osmotic adjustment, water relations and carbohydrate remobilization in pigeonpea under water deficits. J. Plant Physiol., 157(6), 651–659. doi: 10.1016/S0176-1617(00)80008-5

Moshelion, M., Halperin, O., Wallach, R., Oren, R., & Way, D. A. (2015). Role of aquaporins in determining transpiration and photosynthesis in water-stressed plants: crop water-use efficiency, growth and yield. Plant Cell Environ., 38(9), 1785–1793. doi: 10.1111/pce.12410

Jang, J. Y., Kim, D. G., Kim, Y. O., Kim, J. S., & Kang, H. (2004). An expression analysis of a gene family encoding plasma membrane aquaporins in response to abiotic stresses in Arabidopsis thaliana. Plant Mol. Biol., 54(5), 713–725. doi: 10.1023/B:PLAN.0000040900.61345.a6

Surbanovski, N., Sargent, D. J., Else, M. A., Simpson, D. W., Zhang, H., & Grant, O. M. (2013). Expression of Fragaria vesca PIP aquaporins in response to drought stress: PIP down-regulation correlates with the decline in substrate moisture content. PLoS One, 8(9), e74945. doi: 10.1371/journal.pone.0074945

Yue, C., Cao, H., Wang, L., Zhou, Y., Hao, X., Zeng, J., Wang, X., & Yang, Y. (2014). Molecular cloning and expression analysis of tea plant aquaporin (AQP) gene family. Plant Physiol. Biochem., 83, 65–76. doi: 10.1016/j.plaphy.2014.07.011

Morillon, R., & Chrispeels, M. J. (2001). The role of ABA and the transpiration stream in the regulation of the osmotic water permeability of leaf cells. Proc. Nat. Acad. Sci. USA., 98(24), 4138–14143. doi: 10.1073/pnas.231471998

Jang, J. Y., Leem, S. H., Rhee, J. Y., Chung, G. C., Ahn, S. J., & Kang, H. (2007). Transgenic Arabidopsis and tobacco plants overexpressing an aquaporin respond differently to various abiotic stresses. Plant Mol. Biol., 64(6), 621–632. doi: 10.1007/s11103-007-9181-8

Bliuma, D. (2010). Gene expression of the PIP2 subgroup aquaporins in Sium latifolium L. under different water regimes. Naukovi zapysky Ternopilskoho natsionalnoho pedahohichnoho universytetu imeni Volodymyra Hnatiuka. Seriia: Biolohiia [Scientific Issue Ternopil Volodymyr Hnatiuk National Pedagogical University. Series: Biology], 45(4), 3–8. [in Ukrainian]

Zhou, S., Hu, W., Deng, X., Ma, Z., Chen, L., Huang, C., … He, G. (2012). Overexpression of the wheat aquaporin gene, TaAQP7, enhances drought tolerance in transgenic tobacco. PLoS One, 7(12), e52439. doi: 10.1371/journal.pone.0052439

Hachez, C., Zelazny, E., & Chaumont, F. (2006). Modulating the expression of aquaporin genes in planta: a key to understand their physiological functions? Biochim. Biophys. Acta., 1758(8), 1142–1156. doi: 10.1016/j.bbamem.2006.02.017

Carvajal, M., Cooke, D. T., & Clarkson, D. T. (1996). Response of wheat plants to nutrient deprivation may involve the regulation of water uptake. Planta, 199(3), 372–381. doi: 10.1007/BF00195729

Frick, A., Järvå, M., Ekvall, M., Uzdavinys, P., Nyblom, M., & Törnroth-Horsefield, S. (2013). Mercury increases water permeability of a plant aquaporin through a non cysteine-related mechanism. Biochem. J., 454(3), 491–499. doi: 10.1042/BJ20130377

Ho, C., Kelly, M. B., & Stubbs, C. D. (1994). The effects of phospholipid unsaturation and alcohol perturbation at the protein/lipid interface probed using fluorophore lifetime heterogeneity. Biochem. Biophys. Acta, 1193(2), 307–315. doi: 10.1016/0005-2736(94)90167-8

López-Pérez, L., Martínez-Ballesta, M. C., Maurel, C., & Carvajal, M. (2009). Changes in plasma membrane lipids, aquaporins and proton pump of broccoli roots, as an adaptation mechanism to salinity. Phytochem., 70(4), 492–500. doi: 10.1016/j.phytochem.2009.01.014

Da Silveira, M. G., Golovina, E. A., Hoekstra, F. A., Rombouts, F. M., & Abee,, T. (2003). Membrane fluidity adjustments in ethanol-stressed Oenococcus oeni сells. Appl. Environ. Microbiol., 69(10), 5826–5832. doi: 10.1128/AEM.69.10.5826-5832.2003

Luu, D. T., & Maurel, C. (2013). Aquaporin trafficking in plant cells: an emerging membrane-protein model. Traffic, 14(6), 629–635. doi: 10.1111/tra.12062

Belugin, B. V., Zhestkova, I. M., & Trofimova, M. S. (2011). Affinity of PIP aquaporins to sterol enriched domains in plasma membrane of the cells of etiolated pea seedlings. Biochem. (Mosc.) Suppl. Ser. A Membr. Cell Biol., 5(1), 56–63. doi: 10.1134/S1990747810051010

Minami, A., Fujiwara, M., Furuto, A., Fukao, Y., Yamashita, T., Kamo, M., Kawamura, Y., & Uemura, M. (2009). Alterations in detergent-resistant plasma membrane microdomains in Arabidopsis thaliana during cold acclimation. Plant Cell Physiol., 50(2), 341–359. doi: 10.1093/pcp/pcn202

Hachez, C., Besserer, A., Chevalier, A. S., & Chaumont, F. (2013). Insights into plant plasma membrane aquaporin trafficking. Trends Plant Sci., 18(6), 344–352. doi: 10.1016/j.tplants.2012.12.003

Chalbi, N., Martinez-Ballesta, M. C., Youssef, N. B., & Carvajal, M. (2015). Intrinsic stability of Brassicaceae plasma membrane in relation to changes in proteins and lipids as a response to salinity. J. Plant Physiol., 175, 148–156. doi: 10.1016/j.jplph.2014.12.003

Silva, C., Aranda, F. J., Ortiz, A., Carvajal, M., Martínez, V., & Teruel, J. A. (2007). Root plasma membrane lipid changes in relation to water transport in pepper: a response to NaCl and CaCl2 treatment. J. Plant Biol., 50(6), 650–657. doi: 10.1007/BF03030609

Disalvo, E. A. (2015). Membrane hydration: a hint to a new model for biomembranes. Subcell Biochem., 71, 1–16. doi: 10.1007/978-3-319-19060-0_1

Lee, A. G. (2004). How lipids affect the activities of integral membrane proteins. Biochim. Biophys. Acta., 1666(1–2), 62–87. doi: 10.1016/j.bbamem.2004.05.012

Vigh, L., Huitema, H., Woltjes, J., & van Hasselt, P. R. (1986). Drought stress-induce changes in the composition and physical state of phospholipids in wheat. Physiol. Plant., 67(1), 92–96. doi: 10.1111/j.1399-3054.1986.tb01268.x

Navarri-Izzo, F., Quartacci, M. F., Melfi, D., & Izzo, R. (1993). Lipid composition of plasma membranes isolated from sunflower seedlings grown under water stress. Physiol. Plant., 87(4), 508–514. doi: 10.1111/j.1399-3054.1993.tb02500.x