Skip to main content
SpringerLink
Log in

Localization of arabinogalactan-proteins in different stages of embryos and their role in cotyledon formation of Nicotiana tabacum L.

  • Original Article
  • Published:
Sexual Plant Reproduction Aims and scope Submit manuscript

Abstract

Arabinogalactan proteins (AGPs) have been implicated in plant development including sexual plant reproduction. In this paper, the expression of AGPs and the effects of β-glucosyl Yariv reagent (βGlcY, which binds arabinogalactan proteins) in embryo development and cotyledon formation were investigated. Immunofluorescence assay displayed that the expression of AGPs labeled with antibody JIM13 was developmentally regulated. In early stages, AGPs were evenly distributed in the whole embryo, except for a short polar expression in the basal suspensor cell. In the globular stage of embryo, AGPs were condensed in the embryo proper (EP), apex of the EP, and at the juncture of the EP and suspensor. In heart-shaped embryo, APGs were only present at the juncture of the EP and suspensor. Immunogold labeling assay showed that the strong expression of AGPs at the juncture of the EP and suspensor was localized in the cell wall. Provision of βGlcY to the in vitro ovule culture medium caused delayed growth of embryos, cotyledon defect and abnormal venation pattern. Consequently, βGlcY induced the death of defective seedlings with the characteristics of deformed or irregular single cotyledon. Our results suggested that AGPs play functional roles in embryo development, cotyledon formation and seedling morphology establishment in Nicotiana tabacum L.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Abbreviations

AGPs:

Arabinogalactan proteins

DAP:

Days after pollination

EP:

Embryo proper

Mb:

Monoclonal antibodies.

References

  • Aida M, Ishida T, Fukaki H, Fujisawa H, Tasaka M (1997) Gene involved in organ separation in Arabidopsis: an analysis of the cup-shaped cotyledon mutant. Plant Cell 9:841–857

    Article  PubMed  CAS  Google Scholar 

  • Barton MK, Poethig RS (1993) Formation of the shoot apical meristem in Arabidopsis thaliana: An analysis of development in the wild type and in the shoot meristem mutant. Development 119:823–831

    Google Scholar 

  • Bennett SRM, Alvarez J, Bossinger G, Smyth DR (1995) Morphogenesis in pinoid mutants of Arabidopsis thaliana. Plant J 8:505–520

    Article  CAS  Google Scholar 

  • Berleth T, Jürgens G (1993) The role of the monopteros gene in organising the basal body region of the Arabidopsis embryo. Development 118:575–587

    Google Scholar 

  • Blilou I, Xu J, Wildwater M, Willemsen V, Paponov I, Friml J, Heldstra R, Aida M, Plame K, Scheres B (2005) The PIN auxin efflux facilitator network controls growth and patterning in Arabidopsis roots. Nature 433:39–44

    Article  PubMed  CAS  Google Scholar 

  • Bougourd S, Marrison J, Haseloff J (2000) An aniline blue staining procedure for confocal microscopy and 3D imaging of normal and perturbed cellular phenotypes in mature Arabidopsis embryo. Plant J 24:543–550

    Article  PubMed  CAS  Google Scholar 

  • Cassab GI (1998) Plant cell wall proteins. Annu Rev Plant Physiol Plant Mol Biol 49:281–309

    Article  PubMed  CAS  Google Scholar 

  • Chapman A, Blervacq AS, Vasseur J, Hilbert JL (2000) Arabinogalactan-proteins in Cichorium somatic embryogenesis: effect of β-glucosyl Yariv reagent and epitope localization during embryo development. Planta 211:305–314

    Article  PubMed  CAS  Google Scholar 

  • Chaudhury AM, Letham S, Craig S, Dennis ES (1993) Amp1-a mutant with high cytokinin levels and altered embryonic pattern, faster vegetative growth, constitutive photomorphogenesis and precocious flowering. Plant J 4:907–916

    Article  CAS  Google Scholar 

  • Cheung AY, Wu HM (1999) Arabinogalactan proteins in plant sexual reproduction. Protoplasma 208:87–98

    Article  CAS  Google Scholar 

  • Cheung AY, May B, Kawata EE, Gu Q, Wu HM (1993) Characterization of cDNAs for stylar transmitting tissue-specific proline-rich proteins in tobacco. Plant J 3:151–160

    Article  PubMed  CAS  Google Scholar 

  • Conway LJ, Poethig RS (1997) Mutations of Arabidopsis thaliana that transform leaves into cotyledons. Proc Natl Acad Sci USA 94:10209–10214

    Article  PubMed  CAS  Google Scholar 

  • Das S, Pal A (2004) Differential regeneration response in two cotyledon types of Vigna radiata: Histomorphological analysis and effect of (beta)-arabinogalactan. J Plant Biochem Biotechnol 13(2):101–106

    CAS  Google Scholar 

  • Egertsdotter U, Arnold SV (1995) Importance of arabinogalactan proteins for the development of somatic embryos of Norway spruce (Picea abies). Physiol Plant 93:334–345

    Article  CAS  Google Scholar 

  • Endrizzi K, Moussian B, Haecker A, Levin J, Laux T (1996) The SHOOT MERISTEMLESS gene is required for maintenance of undifferentiated cell in Arabidopsis shoot and floral meristems and acts at a different regulatory level than the meristem genes WUSCHEL and ZWILLE. Plant J 10:967–979

    Article  PubMed  CAS  Google Scholar 

  • Geldner N, Richter S, Vieten1 A, Marquardt S, Torres-Ruiz RA, Mayer U, Jürgens1 G (2003) Partial loss-of-function alleles reveal a role for GNOM in auxin transport-related, post-embryonic development of Arabidopsis. Development 131:389–400

    Article  PubMed  CAS  Google Scholar 

  • Hall Q, Cannon MC (2002) The cell wall hydroxyproline-rich glycoprotein RSH is essential for normal embryo development in Arabidopsis. Plant Cell 14:1161–1172

    Article  PubMed  CAS  Google Scholar 

  • Hu Y, Qin Y, Zhao J (2006) Localization of an arabinogalactan protein epitope and the effects of Yariv phenylglycoside during zygotic embryo development of Arabidopsis thaliana. Protoplasma 229:21–31

    Article  PubMed  CAS  Google Scholar 

  • Knox JP (1997) The use of antibodies to study the architecture and developmental regulation of plant cell walls. Int Rev Cytol 171:79–120

    Article  PubMed  CAS  Google Scholar 

  • Kreuger M, van Holst GJ (1993) Arabinogalactan-proteins as essential in somatic embryogenesis of Daucus carota L. Planta 189:243–248

    Article  CAS  Google Scholar 

  • Kreuger M, van Holst GJ (1996) Arabinogalactan proteins and plant differentiation. Plant Mol Biol 30:1077–1086

    Article  PubMed  CAS  Google Scholar 

  • Liu CM, Xu ZH, Chua NH (1993) Auxin polar transport is essential for the establishment of bilateral symmetry during early plant embryogenesis. Plant Cell 5:621–630

    Article  PubMed  CAS  Google Scholar 

  • Lukowitz W, Mayer U, Jürgens G (1996) Cytokinesis in the Arabidopsis embryo involves the syntaxin-related KNOLLE gene product. Cell 84:61–71

    Article  PubMed  CAS  Google Scholar 

  • Majewska-Sawka A, Nothnagel EA (2000) The multiple roles of arabinogalactan proteins in plant development. Plant Physiol 122:3–9

    Article  PubMed  CAS  Google Scholar 

  • Motose H, Sugiyama M, Fukuda H (2004) A proteoglycan mediates inductive interaction during plant vascular development. Nature 429:873–878

    Article  PubMed  CAS  Google Scholar 

  • Okada K, Ueda J, Komaki K, Bell CJ, Shimura Y (1991) Requirement of the auxin polar transport system in early stages of Arabidopsis floral bud formation. Plant Cell 3:667–684

    Article  Google Scholar 

  • Pennell RI, Janniche L, Kjellbom P, Scofield GN, Peart JM, Roberts K (1991) Developmental regulation of a plasma membrane arabinogalactan protein epitope in oilseed rape flowers. Plant Cell 3:1317–1326

    Article  PubMed  CAS  Google Scholar 

  • Rauh RA, Basile DV (2003) Phenovariation induced in Streptocarpus prolixus (Gesneriaceae) by β-glucosyl Yariv reagent. Can J Bot 81:338–344

    Article  CAS  Google Scholar 

  • Roy S, Jauh GY, Hepler PK, Lord EM (1998) Effects of Yariv phenylglycoside on cell wall assembly in the lily pollen tube. Planta 204:450–458

    Article  PubMed  CAS  Google Scholar 

  • Qin Y, Zhao J (2004) The role of arabinogalactan-proteins in sexual reproduction of angiosperms. J Plant Physiol Mol Biol 30:371–378

    CAS  Google Scholar 

  • Qin Y, Zhao J (2006) Localization of arabinogalactan-proteins in egg cells, zygotes and two-celled proembryos and effects of β-D-glucosyl Yariv reagent on egg cell fertilization and zygote division in Nicotiana tabacum L. J Exp Bot, 57:2061–2074

    Article  PubMed  CAS  Google Scholar 

  • Scheres B, Benfey P (1999) Asymmetric cell division in plants. Annu Rev Plant Physiol Plant Mol Biol 50:505–537

    Article  PubMed  CAS  Google Scholar 

  • Schwartz BW, Yeung EC, Meinke DW (1994) Disruption of morphogenesis and transformation of the suspensor in abnormal suspensor mutants of Arabidopsis. Development 120:3235–3245

    CAS  Google Scholar 

  • Showalter AM (1993) Structure and function of plant cell wall proteins. Plant Cell 5:9–23

    Article  PubMed  CAS  Google Scholar 

  • Showalter AM (2001) Arabinogalactan-proteins: structure, expression and function. Cell Mol Life Sci 58:1399–1417

    Article  PubMed  CAS  Google Scholar 

  • Souer E, van Houwelingen A, Kloos D, Mol J, Koes R (1996) The No Apical Meristem gene of petunia is required for pattern formation in embryos and flowers and is expressed at meristem and primordia boundaries. Cell 85:159–170

    Article  PubMed  CAS  Google Scholar 

  • Stacey NJ, Roberts K, Knox JP (1990) Patterns of expression of the JIM4 arabinogalactan-protein epitope in cell cultures and during somatic embryogenesis in Daucus carota L. Planta 180:285–292

    Article  CAS  Google Scholar 

  • Takada S, Hibara K, Ishida T, Tasaka M (2001) The CUP-SHAPED COTYLEDON1 gene of Arabidopsis regulates shoot apical meristem formation. Development 128:1127–1135

    PubMed  CAS  Google Scholar 

  • Thompson HJM, Knox JP (1998) Stage-specific responses of embryogenic carrot cell suspension cultures to arabinogalactan protein-binding β-glucosyl Yariv reagent. Planta 205:32–38

    Article  CAS  Google Scholar 

  • Torres-Ruiz RA, Jürgens G (1994) Mutations in the FASS gene uncouple pattern formation and morphogenesis in Arabidopsis development. Development 120:2967–2978

    PubMed  CAS  Google Scholar 

  • Torres-Ruiz RA, Lohner A, Jürgens G (1996) The GURKE gene is required for normal organization of the apical region in the Arabidopsis embryo. Plant J 10:1005–1016

    Article  PubMed  CAS  Google Scholar 

  • Tykarska T (1979) Rape embryogenesis. II. Development of embryo proper. Acta Soc Bot Pol 48:391–421

    Google Scholar 

  • Vernon DM, Hannon MJ, Le M, Forsthoefel NR (2001) An expanded role for the TWN1 gene in embryogenesis: defects in cotyledon pattern and morphology in the twn1 mutant of Arabidopsis (Brassicaceae). Am J Bot 88:570–582

    Article  PubMed  CAS  Google Scholar 

  • Vroemen C, de Vries S, Quatrano R (1999) Signalling in plant embryos during the establishment of the polar axis. Semin Cell Dev Bio 10:157–164

    Article  CAS  Google Scholar 

  • Vroemen CW, Mordhorst AP, Albrecht C, Kwaaitaal MA, de Vries SC (2003) The CUP-SHAPED COTYLEDON3 gene is required for boundary and shoot meristem formation in Arabidopsis. Plant Cell 15:1563–1577

    Article  PubMed  CAS  Google Scholar 

  • Yadegari R, Depaiva GR, Laux T, Koltunow AM, Apuya N, Zimmerman JL, Fischer RL, Harada JJ, Goldberg RB (1994) Cell differentiation and morphogenesis are uncoupled in Arabidopsis raspberry embryos. Plant Cell 6:1713–1729

    Article  PubMed  CAS  Google Scholar 

  • Zhang JZ, Somerville CR (1997) Suspensor-derived polyembryony caused by altered expression of valyl-tRNA synthase in the twn2 mutant of Arabidopsis. Proc Nat Aca Sci USA 94:7349–7355

    Article  CAS  Google Scholar 

  • Zhao J, Mollet JG, Lord EM (2004) Lily (Lilium longiflorum L.) pollen protoplast adhesion is increased in the presence of the peptide SCA. Sex Plant Repord 16:227–233

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The authors thank Dr J.P. Knox (Centre for Plant Sciences, University of Leeds, UK) for the generous gifts of the antibodies. This project was supported the Major State Basic Research Program of China (2007CB108704) and the National Natural Science Foundation of China (30521004, 30770132).

Author information

Authors and Affiliations

  1. Key Laboratory of the Ministry of Education for Plant Developmental Biology, College of Life Sciences, Wuhan University, Wuhan, 430072, China

    Yuan Qin & Jie Zhao

Authors
  1. Yuan Qin
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jie Zhao
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jie Zhao.

Additional information

Communicated by Scott Russell.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Qin, Y., Zhao, J. Localization of arabinogalactan-proteins in different stages of embryos and their role in cotyledon formation of Nicotiana tabacum L.. Sex Plant Reprod 20, 213–224 (2007). https://doi.org/10.1007/s00497-007-0058-4

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00497-007-0058-4

Keywords

Search

Navigation