Biologia plantarum 57:193-198, 2013 | DOI: 10.1007/s10535-012-0266-0
Aquaporin expression during seed osmopriming and post-priming germination in spinach
- 1 Department of Horticulture, Iowa State University, Ames, USA
- 2 Seed Science Center, Iowa State University, Ames, USA
Aquaporins (AQPs) are proteinaceous channels known to regulate transmembrane water transport, and therefore may be important component of imbibition during osmopriming and germination. To explore the association between AQPs and osmopriming-led enhanced germination performance, we studied the expression patterns of four spinach (Spinacia oleracea) AQP coding genes (SoPIP1;1, SoPIP1;2, SoPIP2;1, and SoδTIP) during osmopriming and subsequent germination under optimal conditions, chilling and drought. All these genes were up-regulated within 2-4 d of priming (phase II-imbibition). We hypothesize such up-regulation to facilitate the pressure potential-driven cell expansion and increase germination potential of primed seeds. Our data during post-priming germination suggest that SoPIP1;1 and SoδTIP were more closely associated with enhanced germination performance. In general, all AQPs were downregulated under chilling and drought. However, under chilling, SoPIP2;1 was expressed at relatively higher level in primed seeds that also exhibited greater chilling tolerance, while SoPIP1;2 and SoδTIP exhibited opposite pattern. Similarly, SoPIP1;1, SoPIP2;1, and SoδTIP exhibited higher expression in primed seeds that also had greater drought tolerance.
Keywords: chilling; drought; plasma membrane intrinsic protein; polyethylene glycol; tonoplast intrinsic protein
Subjects: aquaporin; osmopriming; germination; temperature low; water stress; plasma membrane intrinsic protein; tonoplast intrinsic protein; polyethylene glycol; spinach
Received: March 15, 2012; Accepted: May 30, 2012; Published: March 1, 2013 Show citation
References
- Aharon, R., Shahak, Y., Wininger, S., Bendov, R., Kapulnik, Y., Galili, G.: Overexpression of a plasma membrane aquaporin in transgenic tobacco improves plant vigor under favorable growth conditions but not under drought or salt stress. - Plant Cell 15: 439-447, 2003.
Go to original source... - Aroca, R., Amodeo, G., Frenandez-Illescas, S., Herman, E.M., Chaumont, F., Chrispeels, M.J.: The role of aquaporins and membrane damage in chilling and hydrogen peroxide induced changes in the hydraulic conductance of maize roots. - Plant Physiol. 137: 341-353, 2005.
Go to original source... - Baiges, A., Schäffner, A.R., Affenzeller, M.J., Mas, A.: Plant aquaporins. - Physiol. Plant. 115: 175-182, 2002.
Go to original source... - Benamar, A., Tallon, C., Macherel, D.: Membrane integrity and oxidative properties of mitochondria isolated from imbibing pea seeds after priming or accelerated ageing. - Seed Sci. Res. 13: 35-45, 2003.
Go to original source... - Bewley, J.D., Black, M. (ed.): Seeds: Physiology of Development and Germination. 2nd Ed. - Plenum Press, New York 1994.
Go to original source... - Bradford, K.J.: Manipulation of seed water relations via osmotic priming to improve germination under stress conditions. - HortScience 21: 1005-1112, 1986.
Go to original source... - Chen, K., Arora, R.: Dynamics of the antioxidant system during seed osmopriming, post-priming germination, and seedling establishment in spinach (Spinacia oleracea). - Plant Sci. 180: 212-220, 2011.
Go to original source... - Chen, K., Arora, R.: Priming-memory invokes seed stress tolerance. - Environ. exp. Bot. doi: 10.1016/j.envexpbot.2012.03.005
- Chen, K., Arora, R., Arora, U.: Osmopriming of spinach (Spinacia oleracea L. cv. Bloomsdale) seeds and germination performance under temperature and water stress. - Seed Sci. Technol. 38: 36-48, 2010.
Go to original source... - Chen, K., Fessehaie, A., Arora, R.: Dehydrin metabolism is altered during seed osmopriming and subsequent germination under chilling and desiccation in Spinacia oleracea L. cv. Bloomsdale: possible role in stress tolerance. - Plant Sci. 183: 27-36, 2012a.
Go to original source... - Chen, K., Fessehaie, A., Arora, R.: Selection of reference genes for normalizing gene expression during seed priming and germination using qPCR in Zea mays and Spinacia oleracea. - Plant mol. Biol. Rep. 30: 478-487, 2012b.
Go to original source... - De Willigen, C.V., Postaire, O., Tournaire-Roux, C., Boursiac, Y., Maurel, C.: Expression and inhibition of aquaporins in germinating Arabidopsis seeds. - Plant Cell Physiol. 47: 1241-1250, 2006.
Go to original source... - Ermawati, N., Liang, Y.S., Cha, J.-Y., Shin, D., Jung, M.H., Lee, J.J., Lee, B.-H., Han, C.-D., Lee, K.H., Son, D.: A new TIP homolog, ShTIP, from Salicornia shows a different involvement in salt stress compared to that of TIP from Arabidopsis. - Biol. Plant. 53: 271-277, 2009.
Go to original source... - Ernst, M.: Einfluss von Aquaporinen auf die Blattwachstumsdynamik von Nicotiana tabacum (L.) und Arabidopsis thaliana (L.) Heynh. [The effect of aquaporins on the dynamic of Nicotiana tabacum (L.) and Arabidopsis thaliana (L.) Heynh leaf growth.] - PhD Thesis. TU Darmstadt, Darmstadt 2007. [In German]
- Fraysse, L.C., Wells, B., McCann, M.C., Kjellbom, P.: Specific plasma membrane aquaporins of the PIP1 subfamily are expressed in sieve elements and guard cells. - Biol. Cell 97: 519-534, 2005.
Go to original source... - Gallardo, K., Job, C., Groot, S.P.C., Puype, M., Demol, H., Vandekerekhove, J., Job, D.: Proteomic analysis of Arabidopsis seed germination and priming. - Plant Physiol. 126: 835-848, 2001.
Go to original source... - Gao, Y.-P., Young, L., Bonham-Smith, P., Gusta, L.V.: Characterization and expression of plasma and tonoplast membrane aquaporins in primed seeds of Brassica napus during germination under stress conditions. - Plant mol. Biol. 40: 635-644, 1999.
Go to original source... - Hachez, C., Zelazny, E., Chaumont., F.: Modulating the expression of aquaporin genes in planta: a key to understand their physiological functions? - Biochem. biophys. Acta 1758: 1142-1156, 2006.
Go to original source... - Hussain, S.S., Iqbal, M.T., Arif, M.A., Amjad, M.: Beyond osmolytes and transcription factors: drought tolerance in plants via protective proteins and aquaporins. - Biol. Plant. 55: 401-413, 2011.
Go to original source... - Ionenko, I.F., Anisimov, A.V., Dautova, N.R.: Effect of temperature on water transport through aquaporins. - Biol. Plant. 54: 488-494, 2010.
Go to original source... - Ionenko, I.F., Anisimov, A.V., Karimova, F.G.: Water transport in maize roots under the influence of mercuric chloride and water stress: a role of water channels. - Biol. Plant. 50: 74-80, 2006.
Go to original source... - Johansson, I., Larsson, C., Ek, B., Kjellbom, P.: The major integral proteins of spinach leaf plasma membranes are putative aquaporins and are phosphorylated in response to Ca2+ and apoplastic water potential. - Plant Cell 8: 1181-1191, 1996.
Go to original source... - Kaldenhoff, R., Fischer, M.: Aquaporins in plants. - Acta Physiol. 187: 169-176, 2006.
Go to original source... - Karlsson, M., Johansson, I. Bush, M., McCaan, M.C., Maurel, C., Larsson, C., Kjellborn, P.: An abundant TIP expressed in mature highly vacuolated cells. - Plant J. 21: 83-90, 2000.
Go to original source... - Korkmaz, A., Korkmaz, Y.: Promotion by 5-aminolevulenic acid of pepper seed germination and seedling emergence under low-temperature stress. - Sci. Hort. 119: 98-102, 2009.
Go to original source... - Li, D.-D., Tai, F.J., Zhang, Z.T., Li, Y., Zheng, Y., Wu, Y.F., Li, X.B.: A cotton gene encodes a tonoplast aquaporin that is involved in cell tolerance to cold stress. - Gene 438: 26-32, 2009.
Go to original source... - Lian, H.L., Yu, X., Ye, Q., Ding, X.-S., Kitagawa, Y., Kwak, S.-S., Su, W.-A., Tang, Z.C.: The role of aquaporin RWC3 in drought avoidance in rice. - Plant Cell Physiol. 45: 481-489, 2004.
Go to original source... - Ligterink, W., Kodde, J., Lammers, M., Dassen, H., Van der Geest, A.H.M., De Maagd, R.A., Hilhorst, H.W.M.: Stressinducible gene expression and its impact on seed and plant performance: a microarray approach. - In: Adkins, S., Ashmore, S., Navie, S.C. (ed.): Seeds: Biology, Development and Ecology. Pp 139-148. CAB International, Wallingford 2007.
Go to original source... - Lin, W., Peng, Y, Li, G., Arora, R., Tang, Z., Su, W., Cai, W.: Isolation and function characterization of PgTIP1, a hormone-autotrophic cells-specific tonoplast aquaporin in ginseng. - J. exp. Bot. 58: 947-956, 2007.
Go to original source... - 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 Rep. 17: 638-649, 2007.
Go to original source... - Manz, B., Müller, K., Kucera, B., Volke, F., Leubner-Metzger, G.: Water uptake and distribution in germinating tobacco seeds investigated in vivo by nuclear magnetic resonance imaging. - Plant Physiol. 138: 1538-1551, 2005.
Go to original source... - Matsumoto, T., Lian, H.K., Su, W.A., Tanaka, D., Liu, C.W., Iwasaki, I., Kitagawa, Y.: Role of the aquaporin PIP1 subfamily in the chilling tolerance of rice. - Plant Cell Physiol. 50: 216-229, 2009.
Go to original source... - Maurel, C.: Plant aquaporins: novel functions and regulation properties. - FEBS Lett. 581: 2227-2236, 2007.
Go to original source... - Maurel, C., Javot, H., Lauvergeat, V., Gerbeau, P., Tournaire, C., Santoni, V., J. Heyes, J.: Molecular physiology of aquaporins in plants. - Int. Rev. Cytol. 215: 105-148, 2002.
Go to original source... - Maurel, C., Verdoucq, L., Luu, D.-T., Santoni, V.: Plant aquaporins: membrane channels with multiple integrated functions. - Annu. Rev. Plant Biol. 59: 595-624, 2008.
Go to original source... - Nonogaki, H., Chen, F., Bradford, K.J.: Mechanisms and genes involved in germination sensu stricto. - In: Bradford, K.J., Nonogaki, H. (ed.): Seed Development, Dormancy and Germinaton. Pp. 264-304. Blackwell Publishing, Oxford 2007.
Go to original source... - Peng, Y., Arora, R., Li, G., Wang, X., Fessehaie, A.: Rhododendron catawbiense plasma membrane intrinsic proteins are aquaporins, and their over-expression compromises constitutive freezing tolerance and cold acclimation ability of transgenic Arabidopsis plants. - Plant Cell Environ. 31: 1275-1289, 2008.
Go to original source... - Reisen, D., Leborgne-Castel., N., Ozapl, C., Chaumont, F., Marty, F.: Expression of a cauliflower tonoplast aquaporin tagged with GFP in tobacco suspension cells correlates with an increase in cell size. - Plant mol. Biol. 52: 387-400, 2003.
Go to original source... - Shou, H.: Crop improvement through genetic engineering: development of transformation technologies and production of stress tolerant transgenic crops. - Ph.D. Thesis, Iowa State University, Ames 2003.
- Sliwinska, E., Bassel, G.W., Bewley, J.D.: Germination of Arabidopsis thaliana seeds is not completed as a result of elongation of the radicle but of the adjacent transition zone and lower hypocotyls. - J. exp. Bot. 60: 3587-3594, 2009.
Go to original source... - Sung, Y., Cantliffe, D.J., Nagata, R.T., Nascimento, W.M.: Structural changes in lettuce seed during germination at high temperature altered by genotype, seed maturation temperature, and seed priming. - J. amer. Soc. hort. Sci. 133: 300-311, 2008.
Go to original source... - Yu, Q., Hu, Y., Li, J., Wu, Q., Lin, Z.: Sense and antisense expression of plasma membrane aquaporin BnPIP1 from Brassica napus in tobacco and its effects on plant drought resistance. - Plant Sci. 169: 647-656, 2005.
Go to original source...



