PLANT BIOLOGY
ANIMAL BIOLOGY
SUBSCRIPTION
E-SUBSCRIPTION
 
MAP
MAIN PAGE

 

 

 

 

Kirpichnikova А.А., Smirnov P.D., Daneliia G.V., Yemelyanov V.V., Shishova M.F. The plasma membrane and tonoplast PIP and TIP aquaporins abundance during the elongation growth of coleoptile cells of rice seedlings with different growth rates under normoxia and submergence . Sel'skokhozyaistvennaya Biologiya [Agricultural Biology], 2025, Vol. 60, № 3, p. 445-457.
(how to cite this article)

doi: 10.15389/agrobiology.2025.3.445eng

UDC: 633.18:581.1:576.32/.36:577.24

Acknowledgements:
The equipment of the Research Park “Center for Molecular and Cell Technologies” at St. Petersburg State University was used.
Funded by Russian Science Foundation, grant number 22-14-00096, https://rscf.ru/en/project/22-14-00096/

 

THE PLASMA MEMBRANE AND TONOPLAST PIP AND TIP AQUAPORINS ABUNDANCE DURING THE ELONGATION GROWTH OF COLEOPTILE CELLS OF RICE SEEDLINGS WITH DIFFERENT GROWTH RATES UNDER NORMOXIA AND SUBMERGENCE

А.А. Kirpichnikova, P.D. Smirnov, G.V. Daneliia, V.V. Yemelyanov, M.F. Shishova✉

Saint-Petersburg State University, 7-9, Universitetskaya nab., St. Petersburg, 199034 Russia e-mail nastin1972@mail.ru, p.d.smirnov@gmail.com, georgdanelia@gmail.com, bootika@mail.ru, mshishova@mail.ru(✉ corresponding author)

ORCID:
Kirpichnikova А.А. orcid.org/0000-0001-5133-5175
Yemelyanov V.V. orcid.org/0000-0003-2323-5235
Smirnov P.D. orcid.org/0000-0002-4663-8398
Shishova M.F. orcid.org/0000-0003-3657-2986
Daneliia G.V. orcid.org/0009-0005-9330-4840

Final revision received October 31, 2024
Accepted December 12, 2024

Coleoptiles of cereals are characterized by a rather limited time interval of development and perform a protective function. In the hydrophytic cereal rice (Oryza sativa L.), the ability of coleoptile cells to grow by elongation protects the seedling from oxygen deficiency during flooding. Sharp Cell elongation is accompanied by intense vacuolization. This process is due to increased water transport through the plasma membrane and tonoplast, which is carried out by special transporters of the aquaporin group. In the presented work, for the first time, data were obtained that made it possible to reveal a crosslink between changes in the amount of plasma membrane aquaporins of the PIP1 and TIP1 subfamilies and the intensity of cell elongation in coleoptiles of rice seedlings both under normoxia and hypoxia and to reveal the unequal functional significance of plasma membrane and tonoplast aquaporins during cell elongation. The aim of the work was to evaluate the dynamics of the content of aquaporins with predominant localization in the plasma membrane and tonoplast of coleoptile cells during elongation growth in rice under aeration and oxygen deficiency. Seeds of two rice varieties of domestic selection were used: Amethyst (slow-growing) and Kuban 3 (fast-growing). The seeds were surface sterilized and germinated (50 pcs.) under hydroponic conditions in the dark at 29 °С on glass walkways (control plants) or flooded in 750 ml jars using 4 % Knop nutrient solution. Micropreparations were made to determine the length of the cells in the central part of the coleoptiles. They were photographed using a Leica DM 2500 light microscope and a Leica DFC450 C camera (Leica Microsystems GmbH, Germany) at a magnification of 20½. The total microsomal fraction was obtained from coleoptile cells of seedlings at a temperature of 4 °С. The protein content in the samples was determined by the Bradford micromethod using the Coumassie Brilliant Blue G250 dye. The absorption of the dye adsorbed on the proteins was measured on a SPECTROstar Nano plate spectrophotometer (BMG Labtech, Germany) at l = 595 nm. The protein concentration in the samples was determined based on a calibration graph constructed using a solution of egg albumin in 150 mM sucrose and 10 mM Tris-MES. The proteins were separated by denaturing electrophoresis in 10% polyacrylamide gel. The content of aquaporins PIP1 with predominant localization on in the plasma membrane and TIP1 with predominant localization in the tonoplast in the total microsomal fraction was estimated by immunoblot analysis using specific polyclonal antibodies. Microscopic analysis of the length of cells in the central part of coleoptiles revealed the completion of growth in the seedlings of the Kuban 3 variety on the 5th day of development under aerobic conditions. Elongation of coleoptile cells in the Ametist variety was low intense throughout the tested period. When flooded, coleoptiles of the Kuban 3 variety showed almost 2-fold elongation of cells already on the 3rd day of germination compared to the control. More intensive growth under flooding persisted until the 7th day of germination. In the Ametist variety, the differences revealed on the 3rd day were not as great as in the Kuban 3 variety, but by the 5th day the cell length increased almost 3 times. During cell elongation, the protein content in the fraction of cellular endomembranes changed. Due to a significant increase in cell size on the 5th day after germination, there was an almost 3-fold decrease in the concentration of protein in the microsomal fraction. This process continued, although not so intensively, further, by the 7th day of seedling development. A decrease in protein content was noted for both the Kuban 3 and Ametist varieties. Under oxygen deficiency (flooding), it was less pronounced. Using immunoblotting, unequal dynamics of accumulation of proteins of the PIP1 and TIP1 subfamilies aquaporins was shown both during aerobic development of rice seedlings and under oxygen deficiency. The accumulation of PIP1 aquaporins corresponded to a change in the intensity of coleoptile cell elongation. The effect was more visible in the Kuban 3 variety seedlings. However, regardless of the variety and amount of oxygen during germination, the content of vacuolar aquaporins TIP1 gradually increased. The obtained data indicate differences in the functional significance of aquaporins of the plasmalema membrane and tonoplast in the process of elongation growth of coleptile cells under normoxia and oxygen deficiency conditions.

Keywords: aquaporins, submergence, coleoptile, rice Oryza sativa L.

 

REFERENCES

  1. 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 Research, 1985, 25(4): 275-280 CrossRef
  2. 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? Functional Plant Biology, 2016, 43(10): 961-972 CrossRef
  3. Kordan H.A. Patterns of shoot and root growth in rice seedlings germinating under water. Journal of Applied Ecology, 1974, 11(2): 685-690 CrossRef
  4. Voesenek L.A.C.J., Bailey-Serres J. Flood adaptive traits and processes: an overview. New Phytologist, 2015, 206(1): 57-73 CrossRef
  5. Bailey-Serres J., Lee S.C., Brinton E. Waterproofing crops: effective flooding survival strategies. Plant Physiology, 2012, 160(4): 1698-1709 CrossRef
  6. Pucciariello C. Molecular mechanisms supporting rice germination and coleoptile elongation under low oxygen. Plants, 2020, 9(8): 1037 CrossRef
  7. Bogdanova E.M., Bertova A.D., Kirpichnikova A.A., Biktasheva M.O., Kondratieva A.V., Shapiro A.S., Puzanskiy R.K., Korotenko T.L., Mukhina Z.M., Yemelyanov V.V., Shishova M.F. Growth and viability of coleoptiles under oxygen deficiency in Oryza sativa L. from the collection of the Federal rice research center. Sel'skokhozyaistvennaya biologiya [Agricultural Biology], 2023, 58(3): 538-553 CrossRef
  8. Rayle D.L., Cleland R. Enhancement of wall loosening and elongation by acid solution. Plant Physiology, 1970, 46(2): 250-253 CrossRef
  9. Polevoy V.V. Rol’ auksina v sistemakh regulyatsii u rasteniy. XLIV Timiryazevskoe chtenie /Pod redaktsiey M.Kh. Chaylakhyana [The role of auxin in plant regulatory systems. XLIV Timiryazev reading. M.Kh. Chaylakhyan (ed.)]. Leningrad, 1986 (in Russ.).
  10. Kirpichnikova A., Chen T., Teplyakova S., Shishova M. Proton pump and plant cell elongation. Biological Communications, 2018, 63(1): 32-42 CrossRef
  11. Kirpichnikova A.A., Kudoyarova G.R., Emel’yanov V.V., Shishova M.F. Ekologicheskaya genetika, 2023, 21(4): 401-417 CrossRef (in Russ.).
  12. Ali O., Cheddadi I., Landrein B., Long Y. Revisiting the relationship between turgor pressure and plant cell growth. New Phytologist, 2023, 238(1): 62-69 CrossRef
  13. Kurowska M.M. Aquaporins in cereals — important players in maintaining cell homeostasis under abiotic stress. Genes, 2021, 12(4): 47 CrossRef
  14. Kudoyarova G., Veselov D., Yemelyanov V., Shishova M. The role of aquaporins in plant growth under conditions of oxygen deficiency. International Journal of Molecular Sciences, 2022, 23(17): 10159 CrossRef
  15. Daneliya G.V., Emel’yanov V.V., Shishova M.F. Ekologicheskaya genetika, 2024, 22(4): 343-368 CrossRef (in Russ.).
  16. Su Y., Liu Z., Sun J., Wu C., Li Y., Zhang C., Zhao L. Genome-wide identification of maize aquaporin and functional analysis during seed germination and seedling establishment. Frontiers in Plant Science, 2022, 13: 831916 CrossRef
  17. Afzal Z., Howton T.C., Sun Y., Mukhtar M.S. The roles of aquaporins in plant stress responses. Journal of Developmental Biology, 2016, 4(1): 9 CrossRef
  18. Kapilan R., Vaziri M., Zwiazek J.J. Regulation of aquaporins in plants under stress. Biological Research, 2018, 51(1): 4 CrossRef
  19. Groszmann M., Osborn H.L., Evans J.R. Carbon dioxide and water transport through plant aquaporins. Plant, Cell and Environment, 2017, 40(6): 938-961 CrossRef
  20. Yemelyanov V.V., Puzanskiy R.K., Bogdanova E.M., Vanisov S.A., Kirpichnikova A.A., Biktasheva M.O., Mukhina Z.M., Shavarda A.L., Shishova M.F. Alterations in the rice coleoptile metabolome during elongation under submergence stress. International Journal of Molecular Sciences, 2024, 25(24): 13256 CrossRef
  21. Barikina R.P., Devyatov A.G., Veselova T.D. Spravochnik po botanicheskoy mikrotekhnike. Osnovi i metodi [Handbook of botanical microtechnics. Fundamentals and methods]. Moscow, 2004 (in Russ.).
  22. Shishova M.F., Tankelyun O.V., Rudashevskaya E.L., Emel'yanov V.V., Shakhova N.V., Kirpichnikova A.A. 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): 342-352 CrossRef
  23. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry, 1976, 72(1-2): 248-254 CrossRef
  24. Laemmli U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature, 1970, 227(5259): 680-683 CrossRef
  25. Magneschi L., Kudahettige R.L., Alpi A., Perata P. Comparative analysis of anoxic coleoptile elongation in rice varieties: relationship between coleoptile length and carbohydrate levels, fermentative metabolism and anaerobic gene expression. Plant Biology, 2009, 11(4): 561-573 CrossRef
  26. Nghi K.N, Tondelli A., Valè G., Tagliani A., Marè C., Perata P., Pucciariello C. Dissection of coleoptile elongation in japonica rice under submergence through integrated genome-wide association mapping and transcriptional analyses. Plant, Cell and Environment, 2019, 42(6): 1832-1846. CrossRef
  27. Narsai R., Edwards J.M., Roberts T.H., Whelan J., Joss G.H., Atwell B.J. Mechanisms of growth and patterns of gene expression in oxygen-deprived rice coleoptiles. Plant Journal, 2015, 82(1): 25-40 CrossRef
  28. Edwards J.M., Roberts T.H., Atwell B.J. Quantifying ATP turnover in anoxic coleoptiles of rice (Oryza sativa) demonstrates preferential allocation of energy to protein synthesis. Journal of Experimental Botany, 2012, 63(12): 4389-4402 CrossRef
  29. Huang S., Greenway H., Colmer T.D., Millar A.H. Protein synthesis by rice coleoptiles during prolonged anoxia: implications for glycolysis, growth and energy utilization. Annals of Botany, 2005, 96(4): 703-715 CrossRef
  30. Sadiq I., Fanucchi F., Paparelli E., Alpi E., Bachi A., Alpi A., Perata P. Proteomic identification of differentially expressed proteins in the anoxic rice coleoptile. Journal of Plant Physiology, 2011, 168(18): 2234-2243 CrossRef
  31. Atwell B.J., Greenway H., Colmer T.D. Efficient use of energy in anoxia-tolerant plants with focus on germinating rice seedlings. New Phytologist, 2015, 206(1): 36-56 CrossRef
  32. Li Y.S., Ou S.L., Yang C.Y. The seedlings of different japonica rice varieties exhibit differ physiological properties to modulate plant survival rates under submergence stress. Plants (Basel), 2020, 9(8): 982 CrossRef
  33. Lasanthi-Kudahettige R,, Magneschi L,, Loreti E, Gonzali S,, Licausi F,, Novi G,, Beretta O,, Vitulli F., Alpi A., Perata P. Transcript profiling of the anoxic rice coleoptile. Plant Physiol., 2007, 144(1): 218-231 CrossRef
  34. Liu H.Y., Yu X., Cui D.Y., Sun M.H., Sun W.N., Tang Z.C., Kwak S.S., Su W.A. The role of water channel proteins and nitric oxide signaling in rice seed germination. Cell Res., 2007, 17(7): 638-649 CrossRef
  35. Aroca R. Exogenous catalase and ascorbate modify the effects of abscisic acid (ABA) on root hydraulic properties in Phaseolus vulgaris L. plants. J. Plant Growth Regul., 2006, 25: 10-17 CrossRef
  36. Törnroth-Horsefield S., Wang Y., Kjellbom K.P. Structural mechanism of plant aquaporin gating. Nature, 2006, 439: 688-694 CrossRef
  37. Igamberdiev A.U., Hill R.D. Elevation of cytosolic Ca2+ in response to energy deficiency in plants: the general mechanism of adaptation to low oxygen stress. Biochem. J., 2018, 475(8)1411-1425 CrossRef
  38. Jethva J., Schmidt R.R., Sauter M., Selinski J. Try or die: dynamics of plant respiration and how to survive low oxygen conditions. Plants (Basel), 2022, 11(2): 205 CrossRef
  39. Kutschera U., Deng Z., Oses-Prieto J.A., Burlingame A.L., Wang Z.-Y. Cessation of coleoptile elongation and loss of auxin sensitivity in developing rye seedlings: a quantitative proteomic analysis. Plant Signaling and Behavior, 2010, 5(5): 509-517 CrossRef
  40. Kirpichnikova A.A., Biktasheva M.O., Emel’yanov V.V., Shishova M.F. Ekologicheskaya genetika, 2025, 23(1): 5-17 CrossRef (in Russ.).
  41. Li B., Takahashi D., Kawamura Y., Uemura M. Plasma membrane proteome analyses of Arabidopsis thaliana suspension-cultured cells during cold or ABA treatment: relationship with freezing tolerance and growth phase. Journal of Proteomics, 2020, 211: 103528 CrossRef
  42. Mahender A., Anandan A., Pradhan S.K. Early seedling vigour, an imperative trait for direct-seeded rice: an overview on physio-morphological parameters and molecular markers. Planta, 2015, 241(5): 1027-1050 CrossRef
  43. Ray S., Vijayan J., Sarkar R.K. Germination stage oxygen deficiency (GSOD): an emerging stress in the era of changing trends in climate and rice cultivation practice. Front. Plant Sci., 2016, 7: 671 CrossRef

 

back

 


CONTENTS

 

Full article PDF (Rus)