Hostname: page-component-586b7cd67f-t7fkt Total loading time: 0 Render date: 2024-11-22T00:36:20.016Z Has data issue: false hasContentIssue false

Expansin gene expression in Datura ferox L. seeds is regulated by the low-fluence response, but not by the high-irradiance response, of phytochromes

Published online by Cambridge University Press:  22 February 2007

R. Alejandra Mella*
Affiliation:
Cátedra de Fisiología Vegetal, Facultad de Agronomía, Universidad de Buenos Aires and IFEVA, CONICET, Av. San Martin 4453, Buenos Aires, (1417), Argentina
Maria José Burgin
Affiliation:
Cátedra de Fisiología Vegetal, Facultad de Agronomía, Universidad de Buenos Aires and IFEVA, CONICET, Av. San Martin 4453, Buenos Aires, (1417), Argentina
Rodolfo A. Sánchez
Affiliation:
Cátedra de Fisiología Vegetal, Facultad de Agronomía, Universidad de Buenos Aires and IFEVA, CONICET, Av. San Martin 4453, Buenos Aires, (1417), Argentina
*
*Correspondence Fax: +54 0524 11 45148730 Email: [email protected]

Abstract

Expansins are a multi-gene family of proteins involved in changes in cell wall properties. In seeds where the embryo is completely surrounded by the endosperm, dormancy breakage requires weakening of the micropylar endosperm, increased embryo growth potential or both. Cell wall alterations are fundamental components of these processes, and expansins are thought to participate in them. Here, we explore the possible involvement of expansins in the control of germination by phytochrome in Datura ferox L. seeds. Based on the conserved sequences of known expansin genes, corresponding primers were designed to investigate the expression of expansin mRNAs by reverse transcriptase polymerase chain reaction (RT-PCR). One expansin mRNA was detected in micropylar endosperm of D. ferox, while two mRNAs were present in the embryo prior to radicle emergence. Expansin transcript content is promoted by red (R) light, both in the micropylar endosperm and the embryo; these effects of R are far-red light (FR) reversible, displaying a typical low-fluence response (LFR) in a way fully consistent with the photocontrol of germination. On the other hand, when the promotion of germination by the LFR is antagonized by exposing the seeds to continuous FR through a high-irradiance response (HIR) or by ABA, the inhibitory treatments do not affect expansin mRNA abundance. The results support the participation of expansins in the promotion of germination by LFR of phytochromes, and suggest that inhibition of germination by HIR or ABA does not include a reduction in the transcription of expansin genes.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2004

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Benech-Arnold, R.L., Sánchez, R.A., Forcella, F., Kruk, B.C. and Ghersa, C.M. (2000) Environmental control of dormancy in weed seed banks in soil. Field Crops Research 67, 105122.CrossRefGoogle Scholar
Bewley, J.D. and Black, M. (1994) Seeds: Physiology of development and germination (2nd edition). New York, Plenum Press.CrossRefGoogle Scholar
Bewley, J.D., Burton, R.A., Morohashi, Y. and Fincher, G.B. (1997) Molecular cloning of a cDNA encoding a (1–4.)-beta-mannan endohydrolase from the seeds of germinated tomato ( Lycopersicon esculentum ). Planta 203, 454459.CrossRefGoogle ScholarPubMed
Botto, J.F., Sánchez, R.A., Whitelam, G.C. and Casal, J.J. (1996) Phytochrome A mediates the promotion of seed germination by very low fluences of light and canopy shade light in Arabidopsis. Plant Physiology 110, 439444.CrossRefGoogle ScholarPubMed
Bradford, K.J., Chen, F., Cooley, M.B., Dahal, P., Downie, B., Fukunaga, K.K., Gee, O.H., Gurusinghe, S., Mella, R.A., Nonogaki, H., Wu, C-T. and Yim, K.O. (2000) Gene expression prior to radicle emergence in imbibed tomato seeds. pp. 231251. in Black, M.;Bradford, K.J.;Vazquez-Ramos, J. (Eds) Seed biology: Advances and applications. Wallingford, CABI Publishing.Google Scholar
Brummell, D.A., Harpster, M.H. and Dunsmuir, P. (1999) Differential expression of expansin gene family members during growth and ripening of tomato fruit. Plant Molecular Biology 39, 161169.CrossRefGoogle ScholarPubMed
Burgin, M.J., Mella, R.A., Staneloni, R. and Sánchez, R.A. (2000) The transcription of endo-b-mannanase and GA 3b-hydroxylase genes of Datura ferox seeds is regulated by phytochrome. Plant Biology 2000 Abstracts. Annual meeting of the American Society of Plant Physiology – San Diego, USA.Google Scholar
Caderas, D., Muster, M., Vogler, H., Mandel, T., Rose, J.K.C., McQueen-Mason, S. and Kuhlemeier, C. (2000) Limited correlation between expansin gene expression and elongation growth rate. Plant Physiology 123, 13991413.CrossRefGoogle ScholarPubMed
Carpita, N.C., Ross, C.W. and Nabors, M.W. (1979a) The influence of plant growth regulators on the growth of the embryonic axes of red- and far-red- treated lettuce seeds. Planta 145, 511516.CrossRefGoogle ScholarPubMed
Carpita, N.C., Nabors, M.W., Ross, C.W. and Petretic, N.L. (1979b) The growth physics and water relations of red light induced germination in lettuce seeds. III. Changes in the osmotic and pressure potential in the embryonic axes of red and far-red treated seeds. Planta 144, 217224.CrossRefGoogle ScholarPubMed
Casal, J.J. (2002) Environmental cues affecting development. Current Opinion in Plant Biology 5, 3742.CrossRefGoogle ScholarPubMed
Casal, J.J. and Sánchez, R.A. (1998) Phytochromes and seed germination. Seed Science Research 8, 317329.CrossRefGoogle Scholar
Casal, J.J., Sánchez, R.A. Di, Benedetto, A. and de Miguel, L.C. (1991) Light promotion of seed germination in Datura ferox is mediated by a highly stable pool of phytochrome. Photochemistry and Photobiology 53, 249254.CrossRefGoogle Scholar
Casal, J.J., Sánchez, R.A. and Botto, J.F. (1998) Modes of action of phytochromes. Journal of Experimental Botany 49, 127138.Google Scholar
Chen, F. and Bradford, K.J. (2000) Expression of an expansin is associated with endosperm weakening during tomato seed germination. Plant Physiology 124, 12651274.CrossRefGoogle ScholarPubMed
Chen, F., Dahal, P. and Bradford, K.J. (2001) Two tomato expansin genes show divergent expression and localization in embryos during seed development and germination. Plant Physiology 127, 928936.CrossRefGoogle ScholarPubMed
Cho, H.T. and Kende, H. (1997) Expression of expansin genes is correlated with growth in deepwater rice. Plant Cell 9, 16611671.Google Scholar
Corpet, F. (1988) Multiple sequence alignment with hierarchical clustering. Nucleic Acids Research 16, 1088110890.CrossRefGoogle ScholarPubMed
Cosgrove, D.J. (1999) Enzymes and other agents that enhance cell wall extensibility. Annual Review of Plant Physiology and Plant Molecular Biology 50, 391417.CrossRefGoogle ScholarPubMed
Cosgrove, D.J. (2000) Loosening of plant cell walls by expansins. Nature 407, 321326.CrossRefGoogle ScholarPubMed
Dahal, P., Nevins, D.J. and Bradford, K.J. (1997) Relationship of endo-β-mannanase activity and cell wall hydrolysis in tomato endosperm to germination rates. Plant Physiology 113, 12431252.CrossRefGoogle Scholar
de Miguel, L. and Sánchez, R.A. (1992) Phytochrome-induced germination, endosperm softening and embryo growth potential in Datura ferox seeds: Sensitivity to low water potential and time to escape to FR reversal. Journal of Experimental Botany 43, 969974.CrossRefGoogle Scholar
de Miguel, L., Iglesias, L. and Sánchez, R.A. (1999) ABA inhibition of phytochrome-induced germination in Datura ferox L. seeds. Abstracts of the IV International Workshop on Seed Biology, January 1999, Mérida, Yucatan, Mexico Abstract 3:19.Google Scholar
de Miguel, L., Burgin, M.J., Casal, J.J. and Sánchez, R.A. (2000) Antagonistic action of low-fluence and high-irradiance modes of response of phytochrome on germination and β-mannanase activity in Datura ferox seeds. Journal of Experimental Botany 51, 11271133.CrossRefGoogle ScholarPubMed
Halford, W.P. (1999) The essential prerequisites for quantitative RT-PCR. Nature Biotechnology, 17, 835.CrossRefGoogle ScholarPubMed
Hartmann, K.M. (1966) A general hypothesis to interpret “high energy phenomena” of photomorphogenesis on the basis of phytocrome. Photochemistry and Photobiology 5, 349366.CrossRefGoogle Scholar
Hennig, L., Stoddart, W.M., Dieterle, M., Whitelam, G.C. and Schäfer, E. (2002) Phytochrome E controls light-induced germination of Arabidopsis. Plant Physiology 128, 194200.CrossRefGoogle ScholarPubMed
Keller, E. and Cosgrove, D.J. (1995) Expansins in growing tomato leaves. Plant Journal 8, 795802.CrossRefGoogle ScholarPubMed
McQueen-Mason, S.J. and Cosgrove, D.J. (1995) Expansin mode of action on cell walls: analysis of wall hydrolysis, stress relaxation and binding. Plant Physiology 107, 87100.CrossRefGoogle ScholarPubMed
Mella, R.A., Maldonado, S. and Sánchez, R.A. (1995) Phytochrome-induced structural changes and protein degradation prior to radicle protrusion in Datura ferox seeds. Canadian Journal of Botany 73, 13711378.CrossRefGoogle Scholar
Nonogaki, H., Gee, O.H. and Bradford, K.J. (2000) A germination specific endo-β-mannanase gene is expressed in the micropylar endosperm cap of tomato seeds. Plant Physiology 123, 12351245.CrossRefGoogle ScholarPubMed
Psaras, G., Georghiou, K. and Mitrakos, K. (1981) Red-light induced endosperm preparation for radicle protrusion of lettuce embryos. Botanical Gazette 142, 1318.CrossRefGoogle Scholar
Rose, J.K.C., Lee, H.H. and Bennett, A.B. (1997) Expression of a divergent expansin gene is fruit-specific and ripening-regulated. Proceedings of the National Academy of Sciences, USA 94, 59555960.CrossRefGoogle ScholarPubMed
Sánchez, R.A. and de Miguel, L.C. (1985) The effect of red light, ABA and K+ on the growth of Datura ferox embryos and their relations with photocontrol of germination. Botanical Gazette 146, 472476.CrossRefGoogle Scholar
Sánchez, R.A. and de Miguel, L.C. (1997) Phytochrome promotion of mannan-degrading enzyme activities in the micropylar endosperm of Datura ferox seeds requires the presence of the embryo and gibberellin synthesis. Seed Science Research 7, 2733.CrossRefGoogle Scholar
Sánchez, R.A., Sunell, L., Labavitch, J.M. and Bonner, B.A. (1990) Changes in the endosperm cell walls of two Datura species before radicle protrusion. Plant Physiology 93, 8997.CrossRefGoogle ScholarPubMed
Shcherban, T.Y., Shi, J., Durachko, D.M., Guiltnan, M.J., McQueen-Mason, S.J., Shieh, M. and Cosgrove, D.J. (1995) Molecular cloning and sequence analysis of expansins: a highly conserved, multigene family of proteins that mediate cell wall extension in plants. Proceedings of the National Academy of Sciences, USA 92, 92459249.CrossRefGoogle ScholarPubMed
Shichijo, C., Katada, K., Tanaka, O. and Hashimoto, T. (2001) Phytochrome A-mediated inhibition of seed germination in tomato. Planta 213, 764769.CrossRefGoogle ScholarPubMed
Shinomura, T., Nagatani, A., Hanzawa, H., Kubota, M., Watanabe, M. and Furuya, M. (1996) Action spectra for phytochrome A- and phytochrome B-specific photoinduction of seed germination in Arabidopsis thaliana. Proceedings of the National Academy of Sciences, USA 93, 81298133.CrossRefGoogle ScholarPubMed
Shinomura, T., Uchida, K. and Furuya, M. (2000) Elementary processes of photoperception by phytochrome A for high-irradiance response of hypocotyl elongation in Arabidopsis. Plant Physiology 122, 147156.CrossRefGoogle ScholarPubMed
Toorop, P.E., van Aelst, A.C. and Hilhorst, H.W.M. (2000) The second step of the biphasic endosperm cap weakening that mediates tomato ( Lycopersicon esculentum ) seed germination is under the control of ABA. Journal of Experimental Botany 51, 13711379.Google ScholarPubMed
Toyomasu, T., Tsuji, H., Yamane, H., Nakayama, M., Yamaguchi, I., Murofushi, N., Takahashi, N. and Inoue, Y. (1993) Light effects on endogenous levels of gibberellins in photoblastic lettuce seeds. Journal of Plant Growth Regulation 12, 8590.CrossRefGoogle Scholar
Toyomasu, T., Kawaide, H., Mitsuhashi, W., Inoue, Y. and Kamiya, Y. (1998) Phytochrome regulates gibberellin biosynthesis during germination of photoblastic lettuce seeds. Plant Physiology 118, 15171523.CrossRefGoogle ScholarPubMed
Wu, Y.J., Meeley, R.B. and Cosgrove, D.J. (2001) Analysis and expression of the α-expansin and β-expansin gene families in maize. Plant Physiology 126, 222232.CrossRefGoogle ScholarPubMed