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Temporal and spatial appearance of wall polysaccharides during cellularization of barley (Hordeum vulgare) endosperm

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A Protocol for this article was published on 23 August 2012

Abstract

Barley endosperm begins development as a syncytium where numerous nuclei line the perimeter of a large vacuolated central cell. Between 3 and 6 days after pollination (DAP) the multinucleate syncytium is cellularized by the centripetal synthesis of cell walls at the interfaces of nuclear cytoplasmic domains between individual nuclei. Here we report the temporal and spatial appearance of key polysaccharides in the cell walls of early developing endosperm of barley, prior to aleurone differentiation. Flowering spikes of barley plants grown under controlled glasshouse conditions were hand-pollinated and the developing grains collected from 3 to 8 DAP. Barley endosperm development was followed at the light and electron microscope levels with monoclonal antibodies specific for (1→3)-β-d-glucan (callose), (1→3,1→4)-β-d-glucan, hetero-(1→4)-β-d-mannans, arabino-(1→4)-β-d-xylans, arabinogalactan-proteins (AGPs) and with the enzyme, cellobiohydrolase II, to detect (1→4)-β-d-glucan (cellulose). Callose and cellulose were present in the first formed cell walls between 3 and 4 DAP. However, the presence of callose in the endosperm walls was transient and at 6 DAP was only detected in collars surrounding plasmodesmata. (1→3,1→4)-β-d-Glucan was not deposited in the developing cell walls until approximately 5 DAP and hetero-(1→4)-β-d-mannans followed at 6 DAP. Deposition of AGPs and arabinoxylan in the wall began at 7 and 8 DAP, respectively. For arabinoxylans, there is a possibility that they are deposited earlier in a highly substituted form that is inaccessible to the antibody. Arabinoxylan and heteromannan were also detected in Golgi and associated vesicles in the cytoplasm. In contrast, (1→3,1→4)-β-d-glucan was not detected in the cytoplasm in endosperm cells; similar results were obtained for coleoptile and suspension cultured cells.

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Abbreviations

DAP:

Days after pollination

TEM:

Transmission electron microscopy

References

  • Anderson RL (1975) The structure and biosynthesis of endosperm cell wall components. PhD Thesis, LaTrobe University

  • Anderson RL, Clarke AE, Jermyn MA, Knox RB, Stone BA (1978) A carbohydrate-binding arabinogalactan-protein from liquid suspension cultures of Lolium multiflorum endosperm. Aust J Plant Physiol 4:143–158

    Google Scholar 

  • Bacic A, Harris PJ, Stone, BA (1988) Structure and function of plant cell walls. In: Preiss J (ed) The biochemistry of plants, a comprehensive treatise, vol 14. Academic, New York, pp 297–372

  • Bacic A, Stone BA (1981) Chemistry and organization of aleurone cell wall components from wheat and barley. Aust J Plant Physiol 8:475–495

    Article  CAS  Google Scholar 

  • Brown RC, Lemmon BE, Nguyen H (2003) Events during the first four rounds of mitosis establish three developmental domains in the syncytial endosperm of Arabidopsis thaliana. Protoplasma 222:167–174

    Article  PubMed  CAS  Google Scholar 

  • Brown RC, Lemmon BE, Olsen O-A (1994) Endosperm development in barley: microtubule involvement in the morphogenetic pathway. Plant Cell 6:1241–1252

    Article  PubMed  Google Scholar 

  • Brown RC, Lemmon BE, Olsen O-A (1996a) Development of the endosperm in rice (Oryza sativa L.): cellularization. J Plant Res 109:301–313

    Article  Google Scholar 

  • Brown RC, Lemmon BE, Olsen O-A (1996b) Polarization predicts the pattern of cellularization in cereal endosperm. Protoplasma 192:168–177

    Article  Google Scholar 

  • Brown RC, Lemmon BE, Stone BA, Olsen O-A (1997) Cell wall (1→3)- and (1→3, 1→4)- β-glucans during early grain development in rice (Oryza sativa L.). Planta 202:414–426

    Article  PubMed  CAS  Google Scholar 

  • Burton RA, Shirley NJ, King BJ, Harvey AJ, Fincher GB (2004) The CesA gene family of barley. Quantitative analysis of transcripts reveals two groups of co-expressed genes. Plant Physiol 134:224–236

    Article  PubMed  CAS  Google Scholar 

  • Carpita NC (1984) Cell wall development in maize coleoptiles. Plant Physiol 76:205–212

    PubMed  CAS  Google Scholar 

  • Carpita NC, Gibeaut DM (1993) Structural models of primary cell walls in flowering plants: consistency of molecular structure with the physical properties of the walls during growth. Plant J 3:1–30

    Article  PubMed  CAS  Google Scholar 

  • Dhugga KS, Barreiro R, Whitten B, Stecca K, Hazebroek J, Randhawa GS, Dolan M, Kinney AJ, Tomes D, Nichols S, Anderson P (2004) Guar seed beta-mannan synthase is a member of the cellulose synthase super gene family. Science 303:363–366

    Article  PubMed  CAS  Google Scholar 

  • Doblin MS, Vergara CE, Read S, Newbigin EJ, Bacic A (2003) Plant cell wall biosynthesis: making the bricks. In: Rose JC (ed) Annual plant reviews. CRC, Boca Raton, pp 183–222

    Google Scholar 

  • Drea S, Leader DJ, Arnold BC, Shaw P, Dolan L, Doonan JH (2005) Systematic spatial analysis of gene expression during wheat caryopsis development. Plant Cell 17:2172–2185

    Article  PubMed  CAS  Google Scholar 

  • Ferguson C, Teeri TT, Siika-aho M, Read SM, Bacic A (1998) Location of cellulose and callose in pollen tubes and grains of Nicotiana tabacum. Planta 206:452–460

    Article  CAS  Google Scholar 

  • Fincher GB (1975) Morphology and chemical composition of barley endosperm cell walls. J Inst Brew London 81:116–122

    CAS  Google Scholar 

  • Fincher GB, Stone BA (1974) A water-soluble arabinogalactan-peptide from wheat endosperm. Aust J Biol Sci 27:117–132

    CAS  Google Scholar 

  • Fineran BA, Wild DJC, Ingerfeld M (1982) Initial wall formation in the endosperm of wheat, Triticum aestivum: a reevaluation. Can J Bot 60:1776–1795

    Article  Google Scholar 

  • Galun E (1981) Plant protoplasts as physiological tools. Annu Rev Plant Physiol 32:237–266

    Article  CAS  Google Scholar 

  • Gibeaut DM, Pauly M, Bacic A, Fincher GB (2005) Changes in cell wall polysaccharides in developing barley (Hordeum vulgare) coleoptiles. Planta 221:729–738

    Article  PubMed  CAS  Google Scholar 

  • Guillon F, Tranquet O, Quillien L, Utille J-P, Ortiz JJO, Saulnier L (2004) Generation of polyclonal and monoclonal antibodies against arabinoxylans and their use for immunocytochemical location of arabinoxylans in cell walls of endosperm of wheat. J Cereal Sci 40:167–182

    Article  CAS  Google Scholar 

  • Hughes CE (1976) The developing endosperm of Triticum aestivum (L.): an ultrastructural and morphometric study. PhD Thesis, University of Nottingham

  • Johnson K, Jones B, Schultz CJ, Bacic A (2003) Non-enzymic cell wall (glyco)proteins. In: Rose J (ed) The plant cell wall. Blackwell, UK, pp 111–154

    Google Scholar 

  • Jürgens G (2005) Cytokinesis in higher plants. Annu Rev Plant Biol 56:281–299

    Article  PubMed  CAS  Google Scholar 

  • Kimura S, Laosinchai W, Itoh T, Cui X, Linder R, Brown RMJ (1999) Immunogold labeling of rosette terminal cellulose-synthesizing complexes in the vascular plant Vigna angularis. Plant Cell 11:2075–2085

    Article  PubMed  CAS  Google Scholar 

  • Li H, Bacic A, Read SM (1999) Role of callose synthase zymogen in regulating wall deposition in pollen tubes of Nicotiana alata Link et Otto. Planta 208:528–538

    Article  CAS  Google Scholar 

  • Li J, Burton RA, Harvey AJ, Hrmova M, Wardak AZ, Stone BA, Fincher GB (2003) Biochemical evidence linking a putative callose synthase gene with (1→3)-β-d-glucan biosynthesis in barley. Plant Mol Biol 53:213–225

    Article  PubMed  CAS  Google Scholar 

  • Martin DJ, Somers DA (2004) A (1→3)-β-glucanase expressed during oat endosperm development. J Cereal Sci 39:265–272

    Article  CAS  Google Scholar 

  • Mares DJ, Norstog K, Stone BA (1975) Early stages in the development of wheat endosperm. I. The change from free nuclear to cellular endosperm. Aust J Biol Sci 26:813–830

    Google Scholar 

  • Mares DJ, Stone BA, Jeffrey C, Norstog K (1977) Early stages in the development of wheat endosperm. II. Ultrastructural observations on cell wall formation. Aust J Bot 25:599–613

    Article  Google Scholar 

  • McCartney L, Marcus SE, Knox JP (2005) Monoclonal antibodies to plant cell wall xylans and arabinoxylans. J Histochem Cytochem 53:543–546

    Article  PubMed  CAS  Google Scholar 

  • Meikle PJ, Bönig I, Hoogenraad NJ, Clarke AE, Stone BA (1991) The location of (1→3)-β-glucans in the walls of pollen tubes of Nicotiana alata using a (1→3)-β-glucan specific monoclonal antibody. Planta 185:1–8

    Article  CAS  Google Scholar 

  • Meikle PJ, Hoogenraad NJ, Bönig I, Clarke AE, Stone BA (1994) A (1→3, 1→4)-β-glucan-specific monoclonal antibody and its use in the quantitation and immunocytochemical location of (1→3,1→4)-β-d-glucans. Plant J 5:1–9

    Article  PubMed  CAS  Google Scholar 

  • Morrision IN, O’Brien TP (1976) Cytokinesis in the developing wheat grain: division with and without a phragmoplast. Planta 130:57–67

    Article  Google Scholar 

  • Murashige T, Skoog F (1962) A revised method for rapid growth and bioassays with tobacco cultures. Physiol Plant 15:473–479

    Article  CAS  Google Scholar 

  • Olsen O-A, Brown RC, Lemmon BE (1995) Pattern and process of wall formation in developing endosperm. BioEssays 17:803–812

    Article  Google Scholar 

  • Otegui MS, Mastronarde DN, Kang B-H, Bednarek SY, Staehelin LA (2001) Three-dimensional analysis of syncytial-type cell plates during endosperm cellularization visualized by high resolution electron tomography. Plant Cell 13:2033–2051

    Article  PubMed  CAS  Google Scholar 

  • Otegui M, Staehelin A (2000) Syncytial-type cell plates: a novel kind of cell plate involved in endosperm cellularization of Arabidopsis. Plant Cell 12:933–947

    Article  PubMed  CAS  Google Scholar 

  • Pear JR, Kawagoe Y, Schreckengost WE, Delmer DP, Stalker DM (1996) Higher plants contain homologs of the bacterial CELA genes encoding the catalytic subunit of cellulose synthase. Proc Nat Acad Sci USA 93:12637–12642

    Article  PubMed  CAS  Google Scholar 

  • Pettolino FA, Hoogenraad NJ, Ferguson C, Bacic A, Johnson E., Stone BA (2001) A (1→4)-β-mannan-specific monoclonal antibody and its use in the immunocytochemical location of galactomannans. Planta 214:235–242

    Article  PubMed  CAS  Google Scholar 

  • Ranganath RM (2005) Asymmetric cell divisions in flowering plants-one mother, “two-many” daughters. Plant Biol 7:425–448

    Article  PubMed  CAS  Google Scholar 

  • Ridley BL, O’Neill MA, Mohnen DA (2001) Pectins: structure, biosynthesis, and oligogalacturonide-related signaling. Phytochemistry 57:929–967

    Article  PubMed  CAS  Google Scholar 

  • Shibuya N, Iwasaki T (1985) Structural features of rice bran hemicellulose. Phytochemistry 24:285–289

    Article  CAS  Google Scholar 

  • Smallwood M, Yates EA, Willats WGT, Martin H, Knox JP (1996) Immunochemical comparison of membrane-associated and secreted arabinogalactan-proteins in rice and carrot. Planta 198:452–459

    Article  CAS  Google Scholar 

  • Somerville C, Bauer S, Brininstool G, Facette M, Hamann T, Milne J, Osbourne E, Paradez A, Persson S, Raab T, Vorwerk S, Youngs H (2004) Towards a systems approach to understanding cell walls. Science 306:2206–2211

    Article  PubMed  CAS  Google Scholar 

  • Sørensen MB, Mayer U, Lukowitz W, Robert H, Chambrier P, Jürgens G, Somerville C, Lepiniec L, Berger F (2002) Cellularisation in the endosperm of Arabidopsis thaliana is coupled to mitosis and shares multiple components with cytokinesis. Development 129:5567–5576

    Article  PubMed  CAS  Google Scholar 

  • Stone BA, Clarke AE (1992) Chemistry and biology of (1→3)-β-glucans. LaTrobe University Press, Australia

    Google Scholar 

  • Trethewey JAK, Campbell LM, Harris PJ (2005) (1→3,1→4)-β-d-Glucans in the cell walls of the Poales (sensu lato): an immunogold labeling study using a monoclonal antibody. Am J Bot 92:1669–1683

    Article  Google Scholar 

  • Van den Bulck K, Swennen K, Loosveld A-MA, Courtin CM, Brijs K, Proost P, Van Damme J, Van Campenhout S, Mort A, Delcour JA (2005) Isolation of cereal arabinogalactan-peptides and structural comparison of their carbohydrate and peptide moieties. J Cereal Sci 41:59–67

    Article  CAS  Google Scholar 

  • Van Lammeren AAM (1988) Structure and function of the microtubular cytoskeleton during endosperm development in wheat: an immunofluorescence study. Protoplasma 146:18–27

    Article  Google Scholar 

  • Wilkie KCB (1979) The hemicelluloses of cereals and grasses. Adv Carbohydr Chem Biochem 36:215–264

    Article  CAS  Google Scholar 

  • Willats WGT, McCartney L, Mackie W, Knox JP (2001) Pectin: cell biology and prospects for functional analysis. Plant Mol Biol 47:9–27

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This project was funded by the Grains Research and Development Corporation, Australia and a University of Melbourne Early Career Research Grant awarded to S.M. Wilson.

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Correspondence to Antony Bacic.

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Wilson, S.M., Burton, R.A., Doblin, M.S. et al. Temporal and spatial appearance of wall polysaccharides during cellularization of barley (Hordeum vulgare) endosperm. Planta 224, 655–667 (2006). https://doi.org/10.1007/s00425-006-0244-x

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