Skip to main content
Log in

Germin-like genes are expressed during somatic embryogenesis and early development of conifers

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

Germins and germin-like proteins (GLPs) are members of a superfamily of proteins widely distributed in plants. Their localization within the extracellular matrix and in some cases their hydrogen peroxide-producing activity suggests that these proteins are involved in cell wall metabolism during stress responses and developmental processes. Several very highly conserved conifer GLPs have been identified in somatic embryo tissues. In order to gain more knowledge on their potential involvement in the development of this particular tissue, we have characterized a new GLP gene, LmGER1 in hybrid larch. Anti-GLP immunserum and in-gel activity analyses suggested the presence of superoxide dismutase activity in apoplastic proteins from larch somatic embryos. These results could indicate a possible role for LmGER1 in this physiological process. The expression of LmGER1 has been followed during the maturation of somatic embryos and in different organs of young plantlets by homologous transformation with a promoter-gus construct. This promoter was activated in the root cap of young embryos and, later on, in the cotyledons and in the vascular procambium and xylem. Furthermore, the importance of this gene in embryo development was evaluated by transforming embryonal masses with a gene construct encoding a hairpin RNA leading to gene silencing. The potential role of LmGER1 in cross-linking of cell wall components is discussed.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • C Beauchamp I Fridovich (1971) ArticleTitleSuperoxide dismutase: improved assays and an assay applicable to acrylamide gels Anal Biochem 44 276–287 Occurrence Handle4943714 Occurrence Handle1:CAS:528:DyaE38XjtFKhsg%3D%3D Occurrence Handle10.1016/0003-2697(71)90370-8

    Article  PubMed  CAS  Google Scholar 

  • S Becwar R Nagmani R Wann (1990) ArticleTitleInitiation of embryogenic cultures and somatic embryo development in loblolly pine (Pinus taeda) Can J For Res 20 810–817

    Google Scholar 

  • F Bernier A Berna (2001) ArticleTitleGermins and germin-like proteins: plant do-all proteins. But what do they do exactly? Plant Physiol Biochem 39 545–554 Occurrence Handle1:CAS:528:DC%2BD3MXlslGls74%3D Occurrence Handle10.1016/S0981-9428(01)01285-2

    Article  CAS  Google Scholar 

  • SL Bishop-Hurley RC Gardner C Walter (2003) ArticleTitleIsolation and molecular characterization of genes expressed during somatic embryo development in pinus radiata Plant Cell Tissue and Organ Culture 74 267–281 Occurrence Handle1:CAS:528:DC%2BD3sXktlahtbg%3D Occurrence Handle10.1023/A:1024067703550

    Article  CAS  Google Scholar 

  • M Caliskan AC Cuming (1998) ArticleTitleSpatial specificity of H2O2-generating oxalate oxidase gene expression during wheat embryo germination Plant J 15 165–171 Occurrence Handle9721675 Occurrence Handle1:CAS:528:DyaK1cXlslWqtrg%3D Occurrence Handle10.1046/j.1365-313X.1998.00191.x

    Article  PubMed  CAS  Google Scholar 

  • M Caliskan M Turet AC Cuming (2004) ArticleTitleFormation of wheat (Triticum aestivum L.) embryogenic callus involves peroxide-generating germin-like oxalate oxidase Planta 219 132–140 Occurrence Handle14745556 Occurrence Handle1:CAS:528:DC%2BD2cXjs1eisLo%3D Occurrence Handle10.1007/s00425-003-1199-9

    Article  PubMed  CAS  Google Scholar 

  • MA Campbell MH Lara C Jennifer (1998) ArticleTitlePlant Physiol. The characterization of a gene encoding a putative germin-like protein from Solamun tuberosum Plant Physiol 118 711 Occurrence Handle10.1104/pp.118.2.711

    Article  Google Scholar 

  • C Carter RA Graham RW Thornburg (1999) ArticleTitleNectarin I is a novel, soluble germin-like protein expressed in the nectar of Nicotiana sp Plant Mol Biol 41 207–216 Occurrence Handle10579488 Occurrence Handle1:CAS:528:DyaK1MXns1yntb4%3D Occurrence Handle10.1023/A:1006363508648

    Article  PubMed  CAS  Google Scholar 

  • C Carter RW Thornburg (2000) ArticleTitleTobacco nectarin I. Purification and characterization as a germin-like, manganese superoxide dismutase implicated in the defensE of floral reproductive tissues J Biol Chem 275 36726–36733 Occurrence Handle10952990 Occurrence Handle1:CAS:528:DC%2BD3cXoslWmu7k%3D Occurrence Handle10.1074/jbc.M006461200

    Article  PubMed  CAS  Google Scholar 

  • A Christensen H Thordal-Christensen G Zimmermann T Gjetting M Lyngkjær R Dudler P Schweizer (2004) ArticleTitleThe germinlike protein GLP4 exhibits superoxide dismutase activity and is an important component of quantitative resistance in wheat and barley Mol Plant–Microbe Interact 17 109–117 Occurrence Handle14714874 Occurrence Handle1:CAS:528:DC%2BD2cXivVSlt74%3D

    PubMed  CAS  Google Scholar 

  • JM Domon B Dumas E Laine Y Meyer A David H David (1995) ArticleTitleThree glycosylated polypeptides secreted by several embryogenic cell cultures of pine show highly specific serological affinity to antibodies directed against the wheat germin apoprotein monomer Plant Physiol 108 141–148 Occurrence Handle7784502 Occurrence Handle1:CAS:528:DyaK2MXls1Ohsrc%3D Occurrence Handle10.1104/pp.108.1.141

    Article  PubMed  CAS  Google Scholar 

  • B Dumas G Freyssinet KE Pallett (1995) ArticleTitleTissue-specific expression of germin-like oxalate oxidase during development and fungal infection of barley seedlings Plant Physiol 107 1091–1096 Occurrence Handle12228419 Occurrence Handle1:CAS:528:DyaK2MXltVClsr8%3D

    PubMed  CAS  Google Scholar 

  • B Dumas A Sailland JP Cheviet G Freyssinet K Pallett (1993) ArticleTitleIdentification of barley oxalate oxidase as a germin-like protein C R Acad Sci III 316 793–798 Occurrence Handle8044704 Occurrence Handle1:CAS:528:DyaK2cXis1Sgug%3D%3D

    PubMed  CAS  Google Scholar 

  • JM Dunwell (1998) ArticleTitleCupins: a new superfamily of functionally diverse proteins that include germins and plant storage proteins Biotechnol Genet Eng Rev 15 1–32 Occurrence Handle9573603 Occurrence Handle1:CAS:528:DyaK1cXksFemsrk%3D

    PubMed  CAS  Google Scholar 

  • JM Dunwell S Khuri PJ Gane (2000) ArticleTitleMicrobial relatives of the seed storage proteins of higher plants: conservation of structure and diversification of function during evolution of the cupin superfamily Microbiol Mol Biol Rev 64 153–179 Occurrence Handle10704478 Occurrence Handle1:CAS:528:DC%2BD3cXitFygsrw%3D Occurrence Handle10.1128/MMBR.64.1.153-179.2000

    Article  PubMed  CAS  Google Scholar 

  • JM Dunwell A Purvis S Khuri (2004) ArticleTitleCupins: the most functionally diverse protein superfamily? Phytochemistry 65 7–17 Occurrence Handle14697267 Occurrence Handle1:CAS:528:DC%2BD3sXpvFynsro%3D Occurrence Handle10.1016/j.phytochem.2003.08.016

    Article  PubMed  CAS  Google Scholar 

  • J Dyrløv Bendtsen H Nielsen G Heijne Particlevon S Brunak (2004) ArticleTitleImproved prediction of signal peptides: signalP 3.0 J Mol Biol 340 783–795 Occurrence Handle10.1016/j.jmb.2004.05.028 Occurrence Handle1:CAS:528:DC%2BD2cXlt1emu7s%3D

    Article  CAS  Google Scholar 

  • U Egertsdotter S Arnold Particlevon (1995) ArticleTitleImportance of arabinogalactan proteins for the development of somatic embryos of Norway spruce (Picea abies) Physiol Plant 93 334–345 Occurrence Handle1:CAS:528:DyaK2MXjsl2isbc%3D Occurrence Handle10.1111/j.1399-3054.1995.tb02237.x

    Article  CAS  Google Scholar 

  • Z Fan H Gu X Chen H Song Q Wang M Liu LJ Qu Z Chen (2005) ArticleTitleCloning and expression analysis of Zmglp1, a new germin-like protein gene in maize Biochem Biophys Res Commun 331 1257–1263 Occurrence Handle15883011 Occurrence Handle1:CAS:528:DC%2BD2MXjvFelsrw%3D Occurrence Handle10.1016/j.bbrc.2005.04.045

    Article  PubMed  CAS  Google Scholar 

  • LH Filonova PV Bozhkov VB Brukhin G Daniel B Zhivotovsky S Arnold Particlevon (2000) ArticleTitleTwo waves of programmed cell death occur during formation and development of somatic embryos in the gymnosperm, Norway spruce J Cell Sci 113 4399–4411 Occurrence Handle11082033 Occurrence Handle1:CAS:528:DC%2BD3MXmsVKmsg%3D%3D

    PubMed  CAS  Google Scholar 

  • SC Fry (1998) ArticleTitleOxidative scission of plant cell wall polysaccharides by ascorbate-induced hydroxyl radicals Biochem J 332 507–515 Occurrence Handle9601081 Occurrence Handle1:CAS:528:DyaK1cXkt1SqsbY%3D

    PubMed  CAS  Google Scholar 

  • SC Fry J Miller J Dumville (2002) ArticleTitleA proposed role for copper ions in cell wall loosening Plant Soil 247 57–67 Occurrence Handle1:CAS:528:DC%2BD38XovVCmu7w%3D Occurrence Handle10.1023/A:1021140022082

    Article  CAS  Google Scholar 

  • D Gleeson MA Lelu-Walter M Parkinson (2005) ArticleTitleOverproduction of proline in transgenic hybrid larch (Larix×leptoeuropaea (Dengler)) cultures renders them tolerant to cold, salt and frost Mol Breed 15 21–29 Occurrence Handle1:CAS:528:DC%2BD2MXhslyrsrw%3D Occurrence Handle10.1007/s11032-004-1363-3

    Article  CAS  Google Scholar 

  • C Helliwell P Waterhouse (2003) ArticleTitleConstructs and methods for high-throughput gene silencing in plants Methods 30 289–295 Occurrence Handle12828942 Occurrence Handle1:CAS:528:DC%2BD3sXkvVejsrw%3D Occurrence Handle10.1016/S1046-2023(03)00036-7

    Article  PubMed  CAS  Google Scholar 

  • AS Jaikaran TD Kennedy E Dratewka-Kos BG Lane (1990) ArticleTitleCovalently bonded and adventitious glycans in germin J Biol Chem 265 12503–12512 Occurrence Handle2115520 Occurrence Handle1:CAS:528:DyaK3cXlsVOmsbk%3D

    PubMed  CAS  Google Scholar 

  • RA Jefferson TA Kavanagh MW Bevan (1987) ArticleTitleGUS fusions: beta-glucuronidase as a sensitive and versatile gene fusion marker in higher plants Embo J 6 3901–3907 Occurrence Handle3327686 Occurrence Handle1:CAS:528:DyaL1cXovV2itQ%3D%3D

    PubMed  CAS  Google Scholar 

  • L Jones JL Milne D Ashford MC McCann SJ McQueen-Mason (2005) ArticleTitleA conserved functional role of pectic polymers in stomatal guard cells from a range of plant species Planta 221 255–264 Occurrence Handle15578215 Occurrence Handle1:CAS:528:DC%2BD2MXjvVCmsr8%3D Occurrence Handle10.1007/s00425-004-1432-1

    Article  PubMed  CAS  Google Scholar 

  • S Khuri FT Bakker JM Dunwell (2001) ArticleTitlePhylogeny, function, and evolution of the cupins, a structurally conserved, functionally diverse superfamily of proteins Mol Biol Evol 18 593–605 Occurrence Handle11264412 Occurrence Handle1:CAS:528:DC%2BD3MXis1eisbg%3D

    PubMed  CAS  Google Scholar 

  • HJ Kim TC Pesacreta BA Triplett (2004) ArticleTitleCotton-fiber germin-like protein. II: immunolocalization, purification, and functional analysis Planta 218 525–535 Occurrence Handle14634817 Occurrence Handle1:CAS:528:DC%2BD2cXhtFGjtLc%3D Occurrence Handle10.1007/s00425-003-1134-0

    Article  PubMed  CAS  Google Scholar 

  • HJ Kim BA Triplett (2004) ArticleTitleCotton fiber germin-like protein. I. Molecular cloning and gene expression Planta 218 516–524 Occurrence Handle14648117 Occurrence Handle1:CAS:528:DC%2BD2cXhtFGjtb8%3D Occurrence Handle10.1007/s00425-003-1133-1

    Article  PubMed  CAS  Google Scholar 

  • BG Lane (2002) ArticleTitleOxalate, germins, and higher-plant pathogens IUBMB Life 53 67–75 Occurrence Handle12049198 Occurrence Handle1:CAS:528:DC%2BD38XktlGis7c%3D Occurrence Handle10.1080/15216540211474

    Article  PubMed  CAS  Google Scholar 

  • MA Lelu P Label (1994) ArticleTitleChanges in the levels of abscisic acid and its glucose ester conjugate during maturation of hybrid larch (Larix×leptoeuropaea) somatic embryos, in relation to germination and plantlet recovery Physiol Plant 92 53–60 Occurrence Handle1:CAS:528:DyaK2cXmtVWjt7w%3D Occurrence Handle10.1111/j.1399-3054.1994.tb06654.x

    Article  CAS  Google Scholar 

  • MA Lelu G Pilate (2000) Transgenics in Larix M Jain SC Minocha (Eds) Molecular biology of woody plants NumberInSeriesvol 2 Kluwer Academic Publishers Netherlands 119–134

    Google Scholar 

  • MA Lelu K Klimaszewska P Charest (1994) ArticleTitleSomatic embryogenesis from immature and mature zygotic embryos and from cotyledons and needles of somatic plantlets of Larix Can J For Res 24 100–106

    Google Scholar 

  • F Lo Schiavo G Giuliano S Vries Particlede A Genga R Bollini L Pitto F Cozzani V Nuti-Ronchi M Terzi (1990) ArticleTitleA carrot cell variant temperature sensitive for somatic embryogenesis reveals a defect in the glycosylation of extracellular proteins Mol Gen Genet 223 385–393 Occurrence Handle2270078 Occurrence Handle1:CAS:528:DyaK3MXjsFKi Occurrence Handle10.1007/BF00264444

    Article  PubMed  CAS  Google Scholar 

  • M Mathieu G Neutelings S Hawkins E Grenier H David (2003) ArticleTitleCloning of a pine germin-like protein (GLP) gene promoter and analysis of its activity in transgenic tobacco bright yellow 2 cells Physiol Plant 117 425–434 Occurrence Handle12654044 Occurrence Handle1:CAS:528:DC%2BD3sXkslCitrg%3D Occurrence Handle10.1034/j.1399-3054.2003.00050.x

    Article  PubMed  CAS  Google Scholar 

  • N Membré A Berna G Neutelings A David H David D Staiger J Saez Vasquez M Raynal M Delseny F Bernier (1997) ArticleTitlecDNA sequence, genomic organization and differential expression of three Arabidopsis genes for germin/oxalate oxidase-like proteins Plant Mol Biol 35 459–469 Occurrence Handle9349269 Occurrence Handle10.1023/A:1005833028582

    Article  PubMed  Google Scholar 

  • SG Moller MJ McPherson (1998) ArticleTitleDevelopmental expression and biochemical analysis of the Arabidopsis atao1 gene encoding an H2O2-generating diamine oxidase Plant J 13 781–791 Occurrence Handle9681017 Occurrence Handle1:CAS:528:DyaK1cXislejsL8%3D Occurrence Handle10.1046/j.1365-313X.1998.00080.x

    Article  PubMed  CAS  Google Scholar 

  • G Neutelings JM Domon N Membre F Bernier Y Meyer A David H David (1998) ArticleTitleCharacterization of a germin-like protein gene expressed in somatic and zygotic embryos of pine (Pinus caribaea Morelet) Plant Mol Biol 38 1179–1190 Occurrence Handle9869423 Occurrence Handle1:CAS:528:DyaK1MXksVGrtw%3D%3D Occurrence Handle10.1023/A:1006033622928

    Article  PubMed  CAS  Google Scholar 

  • A Ohmiya Y Tanaka K Kadowaki T Hayashi (1998) ArticleTitleCloning of genes encoding auxin-binding proteins (ABP19/20) from peach: significant peptide sequence similarity with germin-like proteins Plant Cell Physiol 39 492–499 Occurrence Handle9664714 Occurrence Handle1:CAS:528:DyaK1cXjsFSmt74%3D

    PubMed  CAS  Google Scholar 

  • A Ros Barcelo (1998) ArticleTitleThe generation of H2O2 in the xylem of Zinnia elegans is mediated by an NADPH-oxidase-like enzyme Planta 207 207–216 Occurrence Handle10.1007/s004250050474

    Article  Google Scholar 

  • J Sambrook E Fritsch T Maniatis (1989) Molecular cloning: a laboratory manual EditionNumber2 Cold Spring Harbor Laboratory Press Cold Spring Harbor, NY

    Google Scholar 

  • M Sanchez MJ Pena G Revilla I Zarra (1996) ArticleTitleChanges in dehydrodiferulic acids and peroxidase activity against ferulic acid associated with cell walls during growth of Pinus pinaster hypocotyl Plant Physiol 111 941–946 Occurrence Handle12226339 Occurrence Handle1:CAS:528:DyaK28XktlKksb0%3D

    PubMed  CAS  Google Scholar 

  • CI Segarra CA Casalongue ML Pinedo VP Ronchi RD Conde (2003) ArticleTitleA germin-like protein of wheat leaf apoplast inhibits serine proteases J Exp Bot 54 1335–1341 Occurrence Handle12709479 Occurrence Handle1:CAS:528:DC%2BD3sXjt1Ogs70%3D Occurrence Handle10.1093/jxb/erg139

    Article  PubMed  CAS  Google Scholar 

  • T Tabuchi T Kumon T Azuma T Nanmori T Yasuda (2003) ArticleTitleThe expression of a germin-like protein with superoxide dismutase activity in the halophyte Atriplex lentiformis is differentially regulated by wounding and abscisic acid Physiol Plant 118 523–531 Occurrence Handle1:CAS:528:DC%2BD3sXmsFWms7g%3D Occurrence Handle10.1034/j.1399-3054.2003.00133.x

    Article  CAS  Google Scholar 

  • EW Thompson BG Lane (1980) ArticleTitleRelation of protein synthesis in imbibing wheat embryos to the cell-free translational capacities of bulk mRNA from dry and imbibing embryos J Biol Chem 255 5965–5970 Occurrence Handle7380848 Occurrence Handle1:CAS:528:DyaL3cXks1KgsL4%3D

    PubMed  CAS  Google Scholar 

  • L Vallelian-Bindschedler E Mosinger JP Metraux P Schweizer (1998) ArticleTitleStructure, expression and localization of a germin-like protein in barley (Hordeum vulgare L.) that is insolubilized in stressed leaves Plant Mol Biol 37 297–308 Occurrence Handle9617802 Occurrence Handle1:CAS:528:DyaK1cXjtlalsb8%3D Occurrence Handle10.1023/A:1005982715972

    Article  PubMed  CAS  Google Scholar 

  • P Aderkas Particlevon P Label MA Lelu (2002a) ArticleTitleCharcoal affects early development and hormonal concentrations of somatic embryos of hybrid larch Tree Physiol 22 431–434

    Google Scholar 

  • P Aderkas Particlevon R Rhor B Sunberg M Gutmann N Dumont-Beboux MA Lelu (2002b) ArticleTitleABA and its influence on development of the embryonal root cap, storage product and secondary metabolite accumulation in hybrid larch somatic embryos Plant Cell Tissue Org Cult 69 111–120 Occurrence Handle10.1023/A:1015245627220

    Article  Google Scholar 

  • A Wagner L Phillips RD Narayan JM Moody B Geddes (2005) ArticleTitleGene silencing studies in the gymnosperm species Pinus radiata Plant Cell Rep 24 95–102 Occurrence Handle15662500 Occurrence Handle1:CAS:528:DC%2BD2MXjs1Olsbo%3D Occurrence Handle10.1007/s00299-004-0911-y

    Article  PubMed  CAS  Google Scholar 

  • SV Wesley CA Helliwell NA Smith MB Wang DT Rouse Q Liu PS Gooding SP Singh D Abbott PA Stoutjesdijk SP Robinson AP Gleave AG Green PM Waterhouse (2001) ArticleTitleConstruct design for efficient, effective and high-throughput gene silencing in plants Plant J 27 581–590 Occurrence Handle11576441 Occurrence Handle1:CAS:528:DC%2BD3MXos12ktLo%3D Occurrence Handle10.1046/j.1365-313X.2001.01105.x

    Article  PubMed  CAS  Google Scholar 

  • F Whitmore (1976) ArticleTitleBinding of ferulic acid to cell walls by peroxidases of Pinus elliottii Phytochemistry 15 375–378 Occurrence Handle1:CAS:528:DyaE28XktFOiur4%3D Occurrence Handle10.1016/S0031-9422(00)86826-0

    Article  CAS  Google Scholar 

  • EJ Woo JM Dunwell PW Goodenough AC Marvier RW Pickersgill (2000) ArticleTitleGermin is a manganese containing homohexamer with oxalate oxidase and superoxide dismutase activities Nat Struct Biol 7 1036–1040 Occurrence Handle11062559 Occurrence Handle1:CAS:528:DC%2BD3cXnvVOgsLg%3D Occurrence Handle10.1038/80954

    Article  PubMed  CAS  Google Scholar 

  • T Yamahara T Shiono T Suzuki K Tanaka S Takio K Sato S Yamazaki T Satoh (1999) ArticleTitleIsolation of a germin-like protein with manganese superoxide dismutase activity from cells of a moss, Barbula unguiculata J Biol Chem 274 33274–33278 Occurrence Handle10559202 Occurrence Handle1:CAS:528:DyaK1MXns1aqtbc%3D Occurrence Handle10.1074/jbc.274.47.33274

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to G. Neutelings.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Mathieu, M., Lelu-Walter, M.A., Blervacq, A.S. et al. Germin-like genes are expressed during somatic embryogenesis and early development of conifers. Plant Mol Biol 61, 615–627 (2006). https://doi.org/10.1007/s11103-006-0036-5

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11103-006-0036-5

Keywords

Navigation