Advertisement

Acta Physiologiae Plantarum

, 40:27 | Cite as

Changes in plasma membrane aquaporin gene expression under osmotic stress and blue light in tomato

  • Jana Balarynová
  • Jiří Danihlík
  • Martin FellnerEmail author
Original Article
  • 244 Downloads

Abstract

Divergent abiotic stresses induce osmotic stress on plant cells resulting in an imbalance in water homeostasis which is preserved by aquaporins. Since the plasma membrane aquaporins (PIPs) were shown to be involved in seed development and responses to abiotic stresses, we focused on determining the contribution of mannitol-induced osmotic stress, blue light (BL), and 7B-1 mutation to their gene expression in tomato (Solanum lycopersicum L.) seeds. To assess that, we used a quantitative RT-PCR to determine the expression profiles of genes encoding PIPs. Subsequently, a multiple linear regression analysis was used to evaluate the impact of studied stressors (mannitol and BL) and 7B-1 mutation on PIP gene expressions. We found that mannitol-induced osmotic stress and 7B-1 mutation (conferring the lower responsiveness to osmotic stress- and BL-induced inhibition of seed germination) decreased expression of PIP1;3, PIP2;3 and PIP1;2, PIP2;1 genes, respectively. This might be a way to retain water for radicle elongation and seed germination under the stress conditions. Interestingly, the expression of PIP1;3 gene was downregulated not only by osmotic stress, but also by BL. Altogether, our data indicate the existence of a link between osmotic stress and BL signalling and the involvement of the 7B-1 mutation in this crosstalk.

Keywords

Tomato Seed Aquaporins Blue light 7B-1 mutant Mannitol PIP

Notes

Acknowledgements

The authors thank Tomáš Fürst for the critical comments about statistical analysis. We thank Renáta Plotzová and Věra Chytilová for technical assistance. We thank Vipen K. Sawhney for providing 7B-1 mutant seeds and Jan Nauš for measurements of the PFD of the light. This work was supported by Ministry of Education, Youth and Sports of the Czech Republic (Project Nos. ME10020 and LO1204) and Operational Programs Education for Competitiveness-European Social Fund (Project No. CZ.1.07/2.3.00/30.0004).

References

  1. Alexandersson E, Fraysse L, Sjövall-Larsen S, Gustavsson S, Fellert M, Karlsson M, Johanson U, Kjellbom P (2005) Whole gene family expression and drought stress regulation of aquaporins. Plant Mol Biol 59(3):469–484CrossRefPubMedGoogle Scholar
  2. Aroca R, Porcel R, Ruiz-Lozano JM (2012) Regulation of root water uptake under abiotic stress conditions. J Exp Bot 63:43–57CrossRefPubMedGoogle Scholar
  3. Baaziz B, Lopez D, Rabot A, Combes D, Gousset A, Bouzid S, Cochard H, Sakr S, Venisse JS (2012) Light-mediated leaf induction and contribution of both the PIP1s and PIP2s aquaporins in five tree species: walnut (Juglans regia) case study. Tree Physiol 32(4):423–434CrossRefPubMedGoogle Scholar
  4. Bergougnoux V, Hlaváčková V, Plotzová R, Novák O, Fellner M (2009) The 7B-1 mutation in tomato confers a blue light-specific lower sensitivity to coronatine, a toxin produced by Pseudomonas syringae pv. tomato. J Exp Bot 60:1219–1230CrossRefPubMedGoogle Scholar
  5. Cochard H, Venisse JS, Barigah TS, Brunel N, Herbette S, Guilliot A, Tyree MT, Sakr S (2007) Putative role of aquaporins in variable hydraulic conductance of leaves in response to light. Plant Physiol 143(1):122–133CrossRefPubMedPubMedCentralGoogle Scholar
  6. Dekkers BJW, Willems L, Bassel GW, van Bolderen-Veldkamp RP, Ligterink W, Hilhorst HWM, Bentsink L (2012) Identification of reference genes for RT-qPCR expression analysis in arabidopsis and tomato seeds. Plant Cell Physiol 53(1):28–37CrossRefPubMedGoogle Scholar
  7. Fellner M, Sawhney VK (2001) Seed germination in a tomato male-sterile mutant is resistant to osmotic, salt and low-temperature stresses. Theor Appl Genet 102:215–221CrossRefGoogle Scholar
  8. Fellner M, Sawhney VK (2002) The 7B-1 mutant in tomato shows blue-light-specific resistance to osmotic stress and abscisic acid. Planta 214:675–682CrossRefPubMedGoogle Scholar
  9. Fellner M, Zhang R, Pharis RP, Sawhney VK (2001) Reduced de-etiolation of hypocotyl growth in a tomato mutant is associated with hypersensitivity to, and high endogenous levels of, abscisic acid. J Exp Bot 52:725–738CrossRefPubMedGoogle Scholar
  10. Goggin DE, Steadman KJ (2012) Blue and green are frequently seen: responses of seeds to short- and mid-wavelength light. Seed Sci Res 22:27–35CrossRefGoogle Scholar
  11. Hlavinka J, Nauš J, Fellner M (2013) Spontaneous mutation 7B-1 in tomato impairs blue light-induced stomatal opening. Plant Sci 209:75–80CrossRefPubMedGoogle Scholar
  12. Jang JY, Kim DG, Kim YO, Kim JS, 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):713–725CrossRefPubMedGoogle Scholar
  13. Ježilová E, Fellner M, Bergougnoux V, Špundová M (2012) Is the rate of photosynthesis under blue light altered in the 7B-1 tomato mutant? Photosynthetica 50:477–480CrossRefGoogle Scholar
  14. Kaldenhoff R, Eckert M (1999) Features and function of plant aquaporins. J Photochem Photobiol B Biol 52(1):1–6CrossRefGoogle Scholar
  15. Kaldenhoff R, Kölling A, Richter G (1993) A novel blue light-and abscisic acid-inducible gene of Arabidopsis thaliana encoding an intrinsic membrane protein. Plant Mol Biol 23(6):1187–1198CrossRefPubMedGoogle Scholar
  16. Kaldenhoff R, Kölling A, Meyers J, Karmann U, Ruppel G, Richter G (1995) The blue light-responsive AthH2 gene of Arabidopsis thaliana is primarily expressed in expanding as well as in differentiating cells and encodes a putative channel protein of the plasmalemma. Plant J 7(1):87–95CrossRefPubMedGoogle Scholar
  17. Kaldenhoff R, Kölling A, Richter G (1996) Regulation of the Arabidopsis thaliana aquaporin gene AthH2 (PIP1b). J Photochem Photobiol B Biol 36(3):351–354CrossRefGoogle Scholar
  18. Lian HL, Yu X, Ye Q, Ding X, Kitagawa Y, Kwak SS, Su WA, Tang ZC (2004) The role of aquaporin RWC3 in drought avoidance in rice. Plant Cell Physiol 45:481–489CrossRefPubMedGoogle Scholar
  19. Lian HL, Yu X, Lane D, Sun WN, Tang ZC, Su WA (2006) Upland rice and lowland rice exhibited different PIP expression under water deficit and ABA treatment. Cell Res 16(7):651–660CrossRefPubMedGoogle Scholar
  20. Liang WH, Li L, Zhang F, Liu YX, Li MM, Shi HH, Li H, Shang F, Lou C, Lin QT, Li JJ, Yang XG (2013) Effects of abiotic stress, light, phytochromes and phytohormones on the expression of OsAQP, a rice aquaporin gene. Plant Growth Regul 69(1):21–27CrossRefGoogle Scholar
  21. Liu HY, Yu X, Cui DY, Sun MH, Sun WN, Tang ZC, Kwak SS, Su WA (2007) The role of water channel proteins and nitric oxide signaling in rice seed germination. Cell Res 17:638–649CrossRefPubMedGoogle Scholar
  22. Liu C, Li C, Liang D, Ma F, Wang S, Wang P, Wang R (2013) Aquaporin expression in response to water-deficit stress in two Malus species: relationship with physiological status and drought tolerance. Plant Growth Regul 70(2):187–197CrossRefGoogle Scholar
  23. Lorenz A, Kaldenhoff R, Hertel R (2003) A major integral protein of the plant plasma membrane binds flavin. Protoplasma 221(1):19–30CrossRefPubMedGoogle Scholar
  24. Lovdal T, Lillo C (2009) Reference gene selection for quantitative real-time PCR normalization in tomato subjected to nitrogen, cold, and light stress. Anal Biochem 237:238–242CrossRefGoogle Scholar
  25. Luu DT, Maurel C (2005) Aquaporins in a challenging environment: molecular gears for adjusting plant water status. Plant Cell Environ 28(1):85–96CrossRefGoogle Scholar
  26. Maurel C, Boursiac Y, Luu DT, Santoni V, Shahzad Z, Verdoucq L (2015) Aquaporins in plants. Physiol Rev 95(4):1321–1358CrossRefPubMedGoogle Scholar
  27. Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Plant 15:473–497CrossRefGoogle Scholar
  28. Obroucheva NV (2012) Transition from hormonal to nonhormonal regulation as exemplified by seed dormancy release and germination triggering. Russ J Plant Physl 59:591–600CrossRefGoogle Scholar
  29. Obroucheva NV (2013) Aquaporins in seeds. Seed Sci Res 23(4):213–216CrossRefGoogle Scholar
  30. Obroucheva NV, Sinkevich IA, Lityagina SV, Novikova GV (2017) Water relations in germinating seeds. Russ J Plant Physiol 64(4):625–633CrossRefGoogle Scholar
  31. Omidvar V, Fellner M (2015) DNA methylation and transcriptomic changes in response to different lights and stresses in 7B-1 male-sterile tomato. PLoS One 10(4):e0121864CrossRefPubMedPubMedCentralGoogle Scholar
  32. Omidvar V, Mohorianu I, Dalmay T, Fellner M (2015) miRNA regulation of abiotic stress-response in 7B-1 male-sterile tomato mutant. Plant Genome 8:1–13CrossRefGoogle Scholar
  33. Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29(9):e45–e45CrossRefPubMedPubMedCentralGoogle Scholar
  34. Piterková J, Luhová L, Hofman J, Turečková V, Novák O, Petřivalský M, Fellner M (2012) Nitric oxide is involved in light-specific responses of tomato during germination under normal and osmotic stress conditions. Ann Bot 110:767–776CrossRefPubMedPubMedCentralGoogle Scholar
  35. Postaire O, Tournaire-Roux C, Grondin A, Boursiac Y, Morillon R, Schäffner AR, Maurel C (2010) A PIP1 aquaporin contributes to hydrostatic pressure-induced water transport in both the root and rosette of Arabidopsis. Plant Physiol 152(3):1418–1430CrossRefPubMedGoogle Scholar
  36. Pucci A, Picarella ME, Mazzucato A (2017) Phenotypic, genetic and molecular characterization of 7B-1, a conditional male-sterile mutant in tomato. Theor Appl Genet.  https://doi.org/10.1007/s00122-017-2964-7 PubMedGoogle Scholar
  37. Sawhney VK (1997) Genic male sterility. In: Shivanna KR, Sawhney VK (eds) Pollen biotechnology for crop production and improvement. Cambridge University Press, Cambridge, pp 183–198CrossRefGoogle Scholar
  38. Sheoran IS, Dumonceaux T, Datla R, Sawhney VK (2006) Anthocyanin accumulation in the hypocotyl of an ABA-over producing male-sterile tomato (Lycopersicon esculentum) mutant. Physiol Plant 127:681–689CrossRefGoogle Scholar
  39. Sheoran IS, Ross AR, Olson DJ, Sawhney VK (2009) Differential expression of proteins in the wild type and 7B-1 male-sterile mutant anthers of tomato (Solanum lycopersicum): a proteomic analysis. J Proteomics 71:624–636CrossRefPubMedGoogle Scholar
  40. Shiota H, Sudoh T, Tanaka I (2006) Expression analysis of genes encoding plasma membrane aquaporins during seed and fruit development in tomato. Plant Sci 171:277–285CrossRefGoogle Scholar
  41. Tian S, Wang X, Li P, Wang H, Ji H, Xie J, Qiu Q, Shen D, Dong H (2016) Plant aquaporin AtPIP1; 4 links apoplastic H2O2 induction to disease immunity pathways. Plant Physiol 171:1635–1650CrossRefPubMedPubMedCentralGoogle Scholar
  42. Toole EH, Hendricks SB, Borthwick HA, Toole VK (1956) Physiology of seed germination. Annu Rev Plant Physiol 7(1):299–324CrossRefGoogle Scholar
  43. Uehlein N, Lovisolo C, Siefritz F, Kaldenhoff R (2003) The tobacco aquaporin NtAQP1 is a membrane CO2 pore with physiological functions. Nature 425:734–737CrossRefPubMedGoogle Scholar
  44. Uehlein N, Sperling H, Heckwolf M, Kaldenhoff R (2012) The Arabidopsis aquaporin PIP1;2 rules cellular CO2 uptake. Plant Cell Environ 35(6):1077–1083CrossRefPubMedGoogle Scholar
  45. Willigen CV, Postaire O, Tournaire-Roux C, Boursiac Y, Maurel C (2006) Expression and inhibition of aquaporins in germinating Arabidopsis seeds. Plant Cell Physiol 47(9):1241–1250CrossRefGoogle Scholar

Copyright information

© Franciszek Górski Institute of Plant Physiology, Polish Academy of Sciences, Kraków 2018

Authors and Affiliations

  • Jana Balarynová
    • 1
  • Jiří Danihlík
    • 2
  • Martin Fellner
    • 1
    Email author
  1. 1.Laboratory of Growth Regulators, Centre of the Region Haná for Biotechnological and Agricultural Research, Faculty of SciencePalacký University and Institute of Experimental Botany AS CROlomoucCzech Republic
  2. 2.Department of Biochemistry, Faculty of SciencePalacký UniversityOlomoucCzech Republic

Personalised recommendations