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A protective role for the embryo surrounding region of the maize endosperm, as evidenced by the characterisation of ZmESR-6, a defensin gene specifically expressed in this region

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Abstract

A Zea mays cDNA clone, ZmESR-6, was isolated as a gene specifically expressed at the basal region of immature kernels. ZmESR-6 cDNA encoded for a small (11.1 kDa) protein homologous to plant defensins. As for other defensins, the protein contained an N-terminal signal peptide signature and a C-terminal acidic peptide, the mature peptide has a molecular mass of 5.5 kDa. ZmESR-6 was highly expressed in developing kernels but the transcript could not be detected in any other maize tissue. The recombinant ZmESR-6 protein, purified from E. coli, showed strong in vitro inhibitory activity against bacterial and fungal plant pathogens, suggesting a role for ZmESR-6 in plant defence. The distribution of the transcripts was restricted to the embryo surrounding region (ESR) of the kernel. Immunolocalisation experiments revealed, however, that at the grain filling phase ZmESR-6 was accumulated in the placentochalaza-cells, rather than in the ESR cells that produce it. Our results suggest that the ESR has a role in protecting the embryo at the very early stages of seed development, whilst contributes to the general defence mechanism of the kernel at later developmental stages.

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References

  • Azevedo, J.L., Maccheroni, W. Jr., Pereira, J.O. and de Arújo, W.L. 2000 Endophytic microorganisms: a review on insect control and recent advances on tropical plants, Electron. J. Biotechnol. [online], vol. 3, no. 1. Available from: http://www.ejbiotechnology.info/content/vol3/issue1/full/4/index.html. ISSN 0717-3458.

  • Bart, P.H.J.T., Cammue, B.P.A. and Thevissen, K. 2002. Plant defensins. Planta 216: 193–202.

    Article  Google Scholar 

  • Bate, N.J., Niu, X., Wang, Y., Reimann, K.S. and Helentjaris, T.G. 2004. An invertase inhibitor from maize localizes to the embryo surrounding region during early kernel development. Plant Physiol. 134: 246–254.

    Article  PubMed  CAS  Google Scholar 

  • Berrocal-Lobo, M., Segura, A., Moreno, M., López, G., García-Olmedo, F. and Molina, A. 2002. Snakins-2, an antimicrobial peptide from potato whose gene is locally induced by wounding and responds to pathogen infection. Plant Physiol. 128: 951–961.

    Article  PubMed  CAS  Google Scholar 

  • Bonello, J.F., Sevilla-Lecoq, S., Berne, A., Risueño, M.C., Dumas, C. and Rogowsky, P.M. 2002. Esr proteins are secreted by the cells of the embryo surrounding region. J. Exp. Bot. 53: 1559–1568.

    Article  PubMed  CAS  Google Scholar 

  • Broekaert, W.F., Cammue, B.P.A., De Bolle, M.F.C., Thevissen, K., De Samblanx, G.W. and Osborn, R.W. 1997. Antimicrobial peptides in plants. Cri. Rev. Plant Sci. 16: 297–323.

    Article  CAS  Google Scholar 

  • Broekaert, W.F., Terras, F.R.G., Cammue, B.P.A. and Osborn, R.W. 1995. Plant defensins: novel antimicrobial peptides as components of the host defense system. Plant Physiol. 108: 1353–1358.

    Article  PubMed  CAS  Google Scholar 

  • Bruix, M., Jiménez, M.A., Santoro, J., González, C., Colilla, F.J., Méndez, E. and Rico, M. 1993. Solution structure of γ1-H and γ1-P thionins from barley and wheat endosperm determined by 1H-NMR: A structural motif common to toxic arthropod proteins. Biochemistry 32: 715–724.

    Article  PubMed  CAS  Google Scholar 

  • Burr, B., Burr, F. and Matz, E.C. 1994. Mapping genes with recombinant inbreds. In: M. Freeling and V. Walbot (Eds.), The Maize Handbook, Springer Verlag, New York, pp. 249–254.

    Google Scholar 

  • Cai, G., Faleri, C., Del Casino, C., Hueros, G., Thompson, R.D. and Cresti, M. 2002. Subcellular localisation of BETL-1, -2, and -4 in Zea mays L. endosperm. Sex Plant Reprod. 15: 85–98.

    Article  CAS  Google Scholar 

  • Chiang, C.C. and Hadwiger, L.A. 1991. The Fusarium solani-induced expression of a pea gene family encoding high cysteine content proteins. Mol. Plant. Microbe Interact. 4: 324–331.

    PubMed  CAS  Google Scholar 

  • Colilla, F.J., Rocher, A. and Méndez, E. 1990. Gamma-purothionins: aminoacid sequence of two polypeptides of a new family of thionins from wheat endosperm. FEBS Lett. 270: 191–194.

    Article  PubMed  CAS  Google Scholar 

  • Cordts, S., Bantin, J., Wittich, P.E., Kranz, E., Lörz, H. and Dresselhaus, T. 2001. ZmES genes encode peptides with structural homology to defensins and are specifically expressed in the female gametophyte of maize. Plant J. 25: 103–114.

    Article  PubMed  CAS  Google Scholar 

  • Cox, K.H. and Goldberg, R.B. 1988. Analysis of plant gene expression. In: C.H. Shaw (Ed.), Plant Molecular Biology: A Practical Approach, IRL Press, Oxford, pp. 1–35.

    Google Scholar 

  • Davis, R.W., Smith, J.D. and Cobb, B.G. 1990. A light and electron microscope investigation of the transfer cell region of maize caryopses. Can. J. Bot. 68: 471–479.

    Article  Google Scholar 

  • Epple, P., Apel, K. and Bohlmann, H. 1997. ESTs reveal a multigene family for plant defensins in Arabidopsis thaliana. FEBS Lett. 400: 168–172.

    Article  PubMed  CAS  Google Scholar 

  • Fant, F., Vranken, W., Broekaert, W. and Borremans, F. 1998. Determination of the three-dimensional solution structure of Raphanus sativus antifungal protein 1 by NMR. J. Mol. Biol. 279: 257–270.

    Article  PubMed  CAS  Google Scholar 

  • García-Olmedo, F., Carmona, M.J., López-Fando, J.J., Fernández, J.A., Castagnaro, A., Molina, A., Hernández-Lucas, C. and Carbonero, P. 1992. Characterization and analysis of thionin genes. In: Bolls and Meins (Eds.), Genes Involved in Plant Defense. Plant Gene Research Series, Springer-Verlag, Heidelberg, pp. 283–302.

    Google Scholar 

  • García-Olmedo, F., Molina, A., Alamillo, J.M. and Rodríguez-Palenzuela, P. 1998. Plant defense peptides. Biopolymers 47: 479–491.

    Article  PubMed  Google Scholar 

  • Gu, Q., Kawata, E.E., Morse, M.J., Wu, H.M. and Cheung, A.Y. 1992. A flower specific cDNA encoding a novel thionin in tobacco. Mol. Gen. Genet. 234: 89–96.

    PubMed  CAS  Google Scholar 

  • Hancock, R.E.W. and Lehrer, R. 1998. Cationic peptides: a new source of antibiotics. TIBTECH. 16: 82–88.

    CAS  Google Scholar 

  • Hueros, G., Royo, J., Maitz, M., Salamini, F. and Thompson, R.D. 1999. Evidence for factors regulating transfer cell-specific expression in maize endosperm. Plant Mol. Biol. 41: 403–414.

    Article  PubMed  CAS  Google Scholar 

  • Hueros, G., Varotto, S., Salamini, F. and Thompson, R.D. 1995. Molecular characterization of BET1, a gene expressed in the endosperm transfer cells of maize. Plant Cell 7: 747–757.

    Article  PubMed  CAS  Google Scholar 

  • Kang, Z. and Buchenauer, H. 2000. Ultraestructural and inmunocytochemical investigations of pathogen development and host responses in resistant and susceptible wheat spikes infected by Fusarium culmorum. Physiol. Mol. Plant Pathol. 57: 255–268.

    Article  CAS  Google Scholar 

  • Kusmerich, C., de Souza Castro, M., Cruz, J.S., Bloch, C. Jr. and Beirao, P.S.L. 1998. Functional and structural features of γ-zeathionins, a new class of sodium channel blockers. FEBS Lett. 440: 302–306.

    Article  Google Scholar 

  • Lay, F.F., Schirra, H.J., Scanlon, M.J., Anderson, M.A. and Craik, D.J. 2003. The three-dimensional solution structure of NaD1, a new floral defensin from Nicotiana alata and its application to a homology model of the crop defense protein affAFP. J. Mol. Biol. 325: 175–188.

    Article  PubMed  CAS  Google Scholar 

  • Lay, F.M., DeLong, C., Mei, K., Wignes, T. and Fobert, P.R. 2002. Analysis of the DRR230 family of pea defensins: gene expression pattern and evidence of broad host-range antifungal activity. Plant Sci. 163: 855–864.

    Article  Google Scholar 

  • Méndez, E., Moreno, A., Colilla, F., Pelaez, F., Limas, G.G., Méndez, R., Soriano, F., Salinas, M. and DeHaro, C. 1990. Primary structure and inhibition of protein synthesis in eukaryotic cell-free system of a novel thionin, γ-hordothionin, from barley endosperm. Eur. J. Biochem. 194: 533–539.

    Article  PubMed  Google Scholar 

  • Meyer, B., Houlné, G., Pozueta-Romero, J., Schantz, M.L. and Schantz, R. 1996. Fruit-specific expression of a defensin-type gene family in bell pepper. Plant Physiol. 112: 615–622.

    Article  PubMed  CAS  Google Scholar 

  • Milligan, S.B. and Gasser, C.G. 1995. Nature and regulation of pistil-expressed genes in tomato. Plant Mol. Biol. 28:691–711.

    Article  PubMed  CAS  Google Scholar 

  • Molina, A., Ahl Goy, P., Fraile, A., Sánchez-Monge, R. and García -Olmedo, F. 1993. Inhibition of bacterial and fungal plant pathogens by thionins of type I and II. Plant Sci. 92: 169–177.

    Article  CAS  Google Scholar 

  • Moreno, M., Segura, A. and García-Olmedo, F. 1994. Pseudothionin-St1, a potato peptide active against potato pathogens. Eur. J. Biochem. 223: 135–139.

    Article  PubMed  CAS  Google Scholar 

  • Opsahl-Ferstad, H.G., Le Deunff, E., Dumas, C. and Rogow-sky, P.M. 1997. ZmEsr, a novel endosperm-specific gene expressed in a restricted region around the maize embryo. Plant J. 12: 235–246.

    Article  PubMed  CAS  Google Scholar 

  • Osborn, R.W., De Samblanx, G.W., Thevissen, K., Goderis, I., Torrekens, S., Van Leuven, F., Attenborough, S., Rees, S.B. and Broekaert, W.F. 1995. Isolation and characterization of plant defensins from seeds of Asteraceae, Fabaceae, Hippocastanaceae and Saxifragaceae. FEBS Lett. 368: 257–262.

    Article  PubMed  CAS  Google Scholar 

  • Pickard, B.G. and Beachy, R.N 1999. Intercellular connections are developmentally controlled to help move molecules through the plant. Cell, 98: 5–8.

    Article  PubMed  CAS  Google Scholar 

  • Royo, J., Gómez, E. and Hueros, G. 2000. A maize homologue of the bacterial CMP-3-deoxy-D-manno-2-octulosonate (KDO) synthetases. J. Biol. Chem. 275: 24993–24999.

    Article  PubMed  CAS  Google Scholar 

  • Sambrock, J., Fritsch, F.F. and Maniatis, T. 1989. Molecular Cloning: A Laboratory Manual, 2nd ed., Cold Spring Harbor Laboratory Press, Cold Spring Harbor.

    Google Scholar 

  • Santandrea, G., Guo, Y., Ó Connell, T. and Thompson, R.D. 2002. Post-phloem protein trafficking in the maize caryopsis: ZmTRXh1, a thioredoxin specifically expressed in the pedicel parenchyma of Zea mays L., is found predominantly in the placentochalaza. Plant Mol Biol. 50: 743–756.

    Article  PubMed  CAS  Google Scholar 

  • Schel, J.H.N., Kieft, H. and Van Lammeren, A.A.M. 1984. Interactions between embryo and endosperm during early developmental stages of maize caryopses (Zea mays). Can. J. Bot. 62: 2842–2853.

    Article  Google Scholar 

  • Segura, A., Moreno, M., Molina, A. and García-Olmedo, F. 1998. Novel defensin subfamily from spinach. FEBS Lett. 435: 159–162.

    Article  PubMed  CAS  Google Scholar 

  • Serna, A., Maitz, M., Ó Connell, T., Santandrea, G., Thevissen, K., Tienens, K., Hueros, G., Faleri, C., Cai, G., Lottspeich, F. and Thompson, R.D. 2001. Maize endosperm secretes a novel antifungal protein into adjacent maternal tissue. Plant J. 25: 687–698.

    Article  PubMed  CAS  Google Scholar 

  • Sokolov, B.P. and Prockop, D.J. 1994. A rapid and simple PCR-based method for isolation of cDNAs from differentially expressed genes. Nucl. Acids Res. 25: 4009–15.

    Article  Google Scholar 

  • Svinarich, D.M., Gómez, R. and Romero, R. 1997. Detection of human defensins in the placenta. Am. J. Reprod. Inmunol. 38: 252–255.

    CAS  Google Scholar 

  • Terras, F.R.G., Eggermont, K., Kovaleva, V., Raikhel, N.V., Osborn, R.W., Kester, A., Rees, S.B., Torrekens, S., Van Leuven, F., Vanderleyden, J., Cammue, B.P.A. and Broekaert, W.F. 1995. Small cysteine-rich antifungal proteins from radish: their role in host defense. Plant Cell, 7: 573–588.

    Article  PubMed  CAS  Google Scholar 

  • Terras, F.R.G., Schoofs, H.M.E., De Bolle, M.F.C., Van Leuven, F., Rees, S.B., Vanderleyden, J., Cammue, B.P.A. and Broekaert, W.F. 1992. Analysis of two novel classes of antifungal proteins from radish (Raphanus sativus L.) seeds. J. Biol. Chem. 267: 15301–15309.

    PubMed  CAS  Google Scholar 

  • Thomma, B.P.H.J., Cammue, B.P.A. and Thevissen, K. 2002. Plant defensins. Planta 216: 193–202.

    Article  PubMed  CAS  Google Scholar 

  • Thomma, BPHJ, Eggermont, K, Penninckx, I.A.M.A., Maunch-Mani, B., Vogelsang, R., Cammue, B.P.A. and Broekaert, W.F. 1998. Separate jasmonate-dependent and salycylate-dependent defense-response pathways in Arabidopsis are essential for resistance to distinct microbial pathogens. Proc. Natl. Acad. Sci. USA 95: 15107–15111.

    Article  PubMed  CAS  Google Scholar 

  • Thompson, R., Hueros, G., Becker, H. and Maitz, M. 2001. Development and functions of seed transfer cells. Plant Sci. 160: 775–783.

    Article  PubMed  CAS  Google Scholar 

  • Thorne, J.H. 1985. Phloem unloading of C and N assimilates in developing seeds. Annu. Rev. Plant Physiol. 36: 317–343.

    Article  CAS  Google Scholar 

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Authors and Affiliations

  1. Departamento de Biología Celular y Génetica, Universidad de Alcalá, E-28871, Alcala de Henares (Madrid), Spain

    Maite Balandín, Joaquín Royo, Elisa Gómez, Luis M. Muniz & Gregorio Hueros

  2. Departamento de Biotecnología, Escuela Técnica Superior de Ingenieros Agrónomos, Universidad Politécnica, E-28040, Madrid, Spain

    Antonio Molina

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  1. Maite Balandín
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  2. Joaquín Royo
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  3. Elisa Gómez
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  4. Luis M. Muniz
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  6. Gregorio Hueros
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Correspondence to Gregorio Hueros.

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Balandín, M., Royo, J., Gómez, E. et al. A protective role for the embryo surrounding region of the maize endosperm, as evidenced by the characterisation of ZmESR-6, a defensin gene specifically expressed in this region. Plant Mol Biol 58, 269–282 (2005). https://doi.org/10.1007/s11103-005-3479-1

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