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Changes in cell wall polysaccharides in developing barley (Hordeum vulgare) coleoptiles

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Abstract

Cell wall polysaccharides in developing barley coleoptiles were examined using acetic acid–nitric acid extraction, alditol acetate and methylation analyses and enzymatic digestion. The coleoptile cell wall from imbibed grain was rich in pectic polysaccharides (30 mol%), arabinoxylan (25 mol%), cellulose (25 mol%) and xyloglucan (6 mol%), but contained only low levels of (1→3,1→4)-β-D-glucan (1 mol%). During 5 days of coleoptile growth, pectic polysaccharides decreased steadily to about 9 mol%, while (1→3,1→4)-β-D-glucan increased to 10 mol%. Following the cessation of growth of the coleoptiles at about 5 days, (1→3,1→4)-β-D-glucan content rapidly decreased to 1 mol%. The cellulose content of the walls remained at about 35–40 mol% throughout coleoptile growth. Similarly, arabinoxylan content remained essentially constant at 25–30 mol% during growth, although the ratio of substituted to unsubstituted 4-linked xylosyl units decreased from about 4:1 to 1:1. Xyloglucan content ranged from 6 mol% to 10 mol% and the oligosaccharide profile determined using a xyloglucan-specific endoglucanase and MALDI-TOF mass spectrometry indicated that the oligosaccharides XXGG and XXGGG were the principal components, with one and two acetyl groups, respectively, Thus, dramatic changes in wall composition were detected during the growth of barley coleoptiles, both with respect to the relative abundance of individual wall constituents and to the fine structure of the arabinoxylans.

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References

  • Avery GS, Burkholder PR (1936) Polarized growth and cell studies on the Avena coleoptile, phytohormone test object. Bull Torr Bot Club 63:1–15

    Google Scholar 

  • Banik M, Garrett TPJ, Fincher GB (1996) Molecular cloning of cDNAs encoding (1→4)-β-xylan endohydrolases from the aleurone layer of germinated barley (Hordeum vulgare). Plant Mol Biol 31:1163–1172

    Google Scholar 

  • Bleiss W (1994) Time course of phytochrome-mediated changes in growth gradients on coleoptiles of Triticum aestivum L. Planta 192:340–346

    Google Scholar 

  • Burstin J (2000) Differential expression of two barley XET-related genes during coleoptile growth. J Exp Bot 51:847–852

    Google Scholar 

  • Burton RA, Gibeaut DM, Bacic A, Findlay K, Roberts K, Hamilton A, Baulcombe DC, Fincher GB (2000) Virus-induced silencing of a plant cellulose synthase gene. Plant Cell 12:691–705

    Google Scholar 

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

    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  CAS  PubMed  Google Scholar 

  • Carpita NC, Shea EM (1989) Linkage structure of carbohydrates by gas chromatography-mass spectrometry (GC-MS) of partially methylated alditol acetates. In: Bierman CJ, McGinnis GD (eds) Analysis of carbohydrates by GLC and MS. CRC, Boca Raton, pp 157–216

    Google Scholar 

  • Carpita NC, Defernez M, Findlay K, Wells B, Shoue DA, Catchpole G, Wilson RH, McCann MC (2001) Cell wall architecture of the elongating maize coleoptile. Plant Physiol 127:551–565

    Article  CAS  PubMed  Google Scholar 

  • Ciucanu I, Kerek F (1984) A simple and rapid method for the permethylation of carbohydrates. Carbohydr Res 131:209–217

    Google Scholar 

  • Frohlich M, Hodick D, Kutschera U (1994) Thickness and structure of the cell walls in developing rye coleoptiles. J Plant Physiol 144:714–719

    Google Scholar 

  • Fry SC, York WS, Albersheim P, Darvill A, Hayashi T, Joseleau JP, Kato Y, Lorences P, Maclachlan GA, McNeil M, Mort AJ, Reid JSG, Seitz HU, Selvendran RR, Voragen AGJ, White AR (1993) An unambiguous nomenclature for xyloglucan-derived oligosacharides. Physiol Plant 89:1–3

    Google Scholar 

  • Gibeaut DM, Carpita NC (1991) Tracing cell wall biogenesis in intact cells and plants: selective turnover and alteration of soluble and cell wall polysaccharides in grasses. Plant Physiol 97:551–561

    Google Scholar 

  • Guillén R, York WS, Pauly M, An J, Impallomeni G, Albersheim P, Darvill AG (1995) Metabolism of xyloglucan generates xylose-deficient oligosaccharide subunits of this polysaccharide in etiolated peas. Carbohydr Res 277:291–311

    Google Scholar 

  • Harvey AJ, Hrmova M, Fincher GB (2001) Regulation of genes encoding β-D-glucan glucohydrolases in barley (Hordeum vulgare). Physiol Plant 113:108–120

    Google Scholar 

  • Hayashi T (1989) Xyloglucans in the primary cell wall. Annu Rev Plant Physiol Plant Mol Biol 40:139–168

    Google Scholar 

  • Herrera MT, Suarez L, Zarra I (1989) Turnover of β(1–3),(1–4)glucan along the oat coleoptile. Plant Physiol Biochem 27:61–66

    Google Scholar 

  • Inouhe M, Nevins DJ (1998) Changes in the activities and polypeptide levels of exo- and endoglucanases in cell walls during developmental growth of Zea mays coleoptiles. Plant Cell Physiol 39:762–768

    CAS  Google Scholar 

  • Inouhe M, McClellan M, Nevins D (1997) Developmental regulation of polysaccharide metabolism and growth in the primary cell walls of maize. Int J Biol Macromol 21:21–28

    Google Scholar 

  • Jia Z, Qin Q, Darvill AG, York WS (2003) Structure of the xyloglucan produced by suspension-cultured tomato cells. Carbohydr Res 338:1197–1208

    Google Scholar 

  • Kato Y, Iki K, Matsuda K (1981a) Cell-wall polysaccharides of immature barley plants. I. Isolation and characterization of a β-D-glucan. Agric Biol Chem 45:2737–2744

    Google Scholar 

  • Kato Y, Iki K, Matsuda K (1981b) Cell-wall polysaccharides of immature barley plants. II. Characterization of a xyloglucan. Agric Biol Chem 45:2745–2753

    Google Scholar 

  • Kim J-B, Carpita NC (1992) Changes in esterification of the uronic acid groups of cell wall polysaccharides during elongation of maize coleoptiles. Plant Physiol 98:646–653

    CAS  Google Scholar 

  • Kim J-B, Olek AT, Carpita NC (2000) Plasma membrane and cell wall exo-β-D-glucanases in developing maize coleoptiles. Plant Physiol 123:471–485

    Google Scholar 

  • Lee RC, Burton RA, Hrmova M, Fincher GB (2001) Barley arabinoxylan arabinofuranohydrolases: purification, characterization and determination of primary structures from cDNA clones. Biochem J 356:181–189

    Google Scholar 

  • Liptay A, Davidson D (1972) Growth of the barley coleoptile. I. Its relationship to cell number and length in normal and γ-irradiated seedlings. Am J Bot 59:266–269

    Google Scholar 

  • Needs PW, Selvendran RR (1994) A critical assessment of a one-tube procedure for the linkage analysis of polysaccharides as partially methylated alditol acetates. Carbohydr Res 254:229–244

    Google Scholar 

  • Parsons A, Firn RD, Digby J (1988) The role of the coleoptile apex in controlling organ elongation. I. The effects of decapitation and apical incisions. J Exp Bot 39:1331–1341

    Google Scholar 

  • Pauly M, Albersheim P, Darvil A, York WS (1999) Molecular domains of the cellulose/xyloglucan network in the cell walls of higher plants. Plant J 20:629–639

    Google Scholar 

  • Pauly M, Qin Q, Greene H, Albersheim P, Darvill A, York WS (2001) Changes in the structure of xyloglucan during cell elongation. Planta 212:842–850

    Google Scholar 

  • Rose JKC, Braam J, Fry SC, Nishitani K (2002) The XTH family of enzymes involved in xyloglucan endotransglucosylation and endohydrolysis: current perspectives and a new unifying nomenclature. Plant Cell Physiol 43:1421–1435

    Article  CAS  PubMed  Google Scholar 

  • Roulin S, Buchala AJ, Fincher GB (2002) Induction of (1→3,1→4)-β-glucan hydrolases in leaves of dark-incubated barley seedlings. Planta 215:51–59

    Google Scholar 

  • Sakurai N, Masuda Y (1978) Auxin-induced changes in barley coleoptile cell wall composition. Plant Cell Physiol 19:1217–1223

    Google Scholar 

  • Sampedro J, Sieiro C, Revilla G, González-Villa T, Zarra I (2001) Cloning and expression pattern of a gene encoding an a-xylosidase active against xyloglucan oligosaccharides from Arabidopsis. Plant Physiol 126:910–920

    Google Scholar 

  • Schunmann PHD, Smith RC, Lang V, Matthews PR, Chandler PM (1997) Expression of XET-related genes and its relation to elongation in leaves of barley (Hordeum vulgare L.). Plant Cell Environ 20:1439–1450

    Google Scholar 

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

    Google Scholar 

  • Shibuya N, Misaki T (1978a) Polysaccharides and glycoproteins in the rice endosperm cell wall. Agric Biol Chem 42:2259–2266

    Google Scholar 

  • Shibuya N, Misaki T (1978b) Structure of hemicellulose isolated from rice endosperm cell wall: mode of linkages and sequences in xyloglucan, β-glucan and arabinoxylan. Agric Biol Chem 42:2267–2274

    CAS  Google Scholar 

  • Shibuya N, Nakane R (1984) Pectic polysaccharides of rice endosperm cell walls. Phytochemistry 23:1425–1429

    Google Scholar 

  • Shibuya N, Misaki A, Iwasaki T (1983) The structure of arabinoxylan and arabinoglucuronoxylan isolated from rice endosperm cell wall. Agric Biol Chem 47:2223–2230

    Google Scholar 

  • Sims IM, Bacic A (1995) Extracellular polysaccharides from suspension-cultures of Nicotiana plumbaginifolia. Phytochemistry 38:1397–1405

    Article  CAS  Google Scholar 

  • Sims IM, Munro SLA, Currie G, Craik D, Bacic A (1996) Structural characterisation of xyloglucan secreted by suspension–cultured cells of Nicotiana plumbaginifolia. Carbohydr Res 293:147–172

    Google Scholar 

  • Sims IM, Middleton K, Lane AG, Cairns AJ, Bacic A (2000) Characterisation of extracellular polysaccharides from suspension cultures of members of the Poaceae. Planta 210:261–268

    Google Scholar 

  • Smith R, Matthews P, Schunmann P, Chandler P (1996) The regulation of leaf elongation and xyloglucan endotransglycosylase by gibberellin in ‘Himalaya’ barley (Hordeum vulgare L.). J Exp Bot 47:1395–1404

    Google Scholar 

  • Strohmeier M, Hrmova M, Fischer M, Harvey AJ, Fincher GB, Pleiss J (2004) Molecular modelling of family GH16 glycoside hydrolases: potential roles for xyloglucan endotransglucosylases/hydrolases in cell wall modification in the Poaceae. Protein Sci 13:3200–3213

    Google Scholar 

  • Suzuki K, Kitamura S, Kato Y, Itoh T (2000) Highly substituted glucuronoarabinoxylans (hsGAXs) and low-branched xylans show a distinct localization pattern in the tissues of Zea mays L. Plant Cell Physiol 41:948–959

    Google Scholar 

  • Thimann KV, O’Brien TP (1965) Histological studies on the coleoptile. II. Comparative vascular anatomy of coleoptiles of Avena and Triticum. Am J Bot 52:918–923

    Google Scholar 

  • Thomas JR, Darvill AG, Albersheim P (1989) Rhamnogalacturonan I, a pectic polysaccharide that is a component of monocot cell walls. Carbohydr Res 185:279–305

    Article  CAS  Google Scholar 

  • Thomas BR, Inouhe M, Simmons CR, Nevins DJ (2000) Endo-1,3;1,4-β-glucanase from coleoptiles of rice and maize: role in the regulation of plant growth. Int J Biol Macromol 27:145–149

    Google Scholar 

  • Trethewey JAK, Harris PJ (2002) Location of (1→3),(1→4)-β-D-glucans in vegetative cell walls of barley (Hordeum vulgare) using immunogold labelling. New Phytologist 154:347–358

    Google Scholar 

  • Updegraff D (1969) Semimicro determination of cellulose in biological materials. Anal Biochem 32:420–424

    Google Scholar 

  • Viëtor RJ, Kormelink FJM, Angelino SAGF, Voragen AGJ (1994) Substitution patterns of water-unextractable arabinoxylans from barley and malt. Carbohydr Polym 24:113–118

    Google Scholar 

  • Vincken J-P, York WS, Beldman G, Voragen AGJ (1997) Two general branching patterns of xyloglucan, XXXG and XXGG. Plant Physiol 114:9–13

    Google Scholar 

  • Watanabe T, Shida M, Murayama T, Furuyama Y, Nakajima T, Matsuda K (1984) Xyloglucan in cell walls of rice hull. Carbohydr Res 129:229–242

    Google Scholar 

  • Wiedenroth EM, Wernicke G, Hoffman P (1990) Morphological and anatomical characterization of the coleoptile of Triticum aestivum with regard to the evolution of forms with different ploidy levels. Annals Bot 66:531–540

    Google Scholar 

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

    Google Scholar 

  • Woodward JR, Fincher GB (1982) Substrate specificities and kinetic properties of two (1→3),(1→4)-β-D-glucan endo-hydrolases from germinating barley (Hordeum vulgare). Carbohydr Res 106:111–122

    Google Scholar 

  • Wright STC (1961) A sequential growth response to gibberellic acid, kinetin and indolyl-3-acetic acid in the wheat coleoptile (Triticum vulgare L.). Nature 190:699–700

    Google Scholar 

  • Yokoyama R, Rose JKC, Nishitani K (2004) A surprising diversity and abundance of xyloglucan endotransglucosylase/hydrolases in rice. Classification and expression analysis. Plant Physiol 134:1088–1099

    Google Scholar 

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Acknowledgements

This work was supported by grants from the Grains Research and Development Corporation and the Australian Research Council (to G.B.F. and A.B.).

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Authors and Affiliations

  1. Australian Centre for Plant Functional Genomics, School of Agriculture and Wine, University of Adelaide, Waite Campus, Glen Osmond, SA, 5064, Australia

    David M. Gibeaut & Geoffrey B. Fincher

  2. Plant Cell Wall Group, Max-Planck Institut für Molekulare Pflanzenphysiologie, 14424, Potsdam, Germany

    Markus Pauly

  3. Plant Cell Biology Research Centre, School of Botany, University of Melbourne, Parkville, VIC, 3010, Australia

    Antony Bacic

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  1. David M. Gibeaut
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  4. Geoffrey B. Fincher
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Correspondence to Geoffrey B. Fincher.

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Gibeaut, D.M., Pauly, M., Bacic, A. et al. Changes in cell wall polysaccharides in developing barley (Hordeum vulgare) coleoptiles. Planta 221, 729–738 (2005). https://doi.org/10.1007/s00425-005-1481-0

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