Comparative in situ analyses of cell wall matrix polysaccharide dynamics in developing rice and wheat grain

Planta

Volumn 241, Issue 3, 2015, Pages 669-685

  Palmer, Richard ^a,b   Cornuault, Valérie ^b   Marcus, Susan E ^b   Knox, J Paul ^b   Shewry, Peter R ^a   Tosi, Paola ^a,c  

^a ROTHAMSTED RESEARCH   (United Kingdom)

^b UNIVERSITY OF LEEDS   (United Kingdom)

^c UNIVERSITY OF READING   (United Kingdom)

Author keywords

Cell wall; Grain development; Immunodetection; Rice grain; Wheat grain

Indexed keywords

POLYSACCHARIDE;

CELL WALL; COMPARATIVE STUDY; ENDOSPERM; FLUORESCENT ANTIBODY TECHNIQUE; FOOD GRAIN; GROWTH, DEVELOPMENT AND AGING; METABOLISM; ORYZA; WHEAT;

CELL WALL; EDIBLE GRAIN; ENDOSPERM; FLUORESCENT ANTIBODY TECHNIQUE; ORYZA; POLYSACCHARIDES; TRITICUM;

EID: 84925510905     PISSN: 00320935     EISSN: 14322048     Source Type: Journal    
DOI: 10.1007/s00425-014-2201-4     Document Type: Article

References (76)

1. Anderson JW, Baird P, Davis RH, Ferreri S, Knudtson M, Koraym A, Waters V, Williams CL (2009) Health benefits of dietary fiber. Nutr Rev 67:188–205
2. Atmodjo MA, Hao ZY, Mohnen D (2013) Evolving views of pectin biosynthesis. Annu Rev Plant Biol 64:747–779
3. Bates B, Lennox A, Swan G (2011) National diet and nutrition survey. Headline results from years 1 to 2 (combined) of the rolling programme (2008/2009–2009/10). London: The Stationery Office
4. Bingham SA, Williams DRR, Cummings JH (1985) Dietary fiber consumption in Britain—new estimates and their relation to large bowel cancer mortality. Brit J Cancer 52:399–402
5. Bjorck I, Ostman E, Kristensen M, Anson NM, Price RK, Haenen GRMM, Havenaar R, Knudsen KEB, Frid A, Mykkanen H, Welch RW, Riccardi G (2012) Cereal grains for nutrition and health benefits: overview of results from in vitro, animal and human studies in the HEALTHGRAIN project. Trends Food Sci Tech 25:87–100
6. Brown RC, Lemmon BE, Stone BA, Olsen OA (1997) Cell wall (1→3)- and (1→3,1→4)-beta-glucans during early grain development in rice (Oryza sativa L). Planta 202:414–426
7. Burton RA, Fincher GB (2009) (1,3;1,4)-beta-d-glucans in cell walls of the poaceae, lower plants, and fungi: a tale of two linkages. Mol Plant 2:873–882
8. Burton RA, Gidley MJ, Fincher GB (2010) Heterogeneity in the chemistry, structure and function of plant cell walls. Nature Chem Biol 6:724–732
9. Cade JE, Burley VJ, Greenwood DC (2007) Dietary fibre and risk of breast cancer in the UK Women’s Cohort Study. Int J Epidemiol 36:431–438
10. Caffall KH, Mohnen D (2009) The structure, function, and biosynthesis of plant cell wall pectic polysaccharides. Carbohydr Res 344:1879–1900
11. Carpita NC (1984) Cell wall development in maize coleoptiles. Plant Physiol 76:205–212
12. 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
13. Chateigner-Boutin AL, Bouchet B, Alvarado C, Bakan B, Guillon F (2014) The wheat grain contains pectic domains exhibiting specific spatial and development-associated distribution. PLoS One 9(2):e89620
14. Clausen MH, Willats WGT, Knox JP (2003) Synthetic methyl hexagalacturonate hapten inhibitors of antihomogalacturonan monoclonal antibodies LM7, JIM5 and JIM7. Carbohydr Res 338:1797–1800
15. Cochrane MP, Duffus CM (1981) Endosperm cell number in barley. Nature 289:399–401
16. Cui W, Wood PJ (2000) Relationships between structural features, molecular weight and rheological properties of cereal beta-d- glucans. Hydrocolloids Pt 1:159–168
17. Dornez E, Cuyvers S, Holopainen U, Nordlund E, Poutanen K, Delcour JA, Courtin CM (2011) Inactive fluorescently labeled xylanase as a novel probe for microscopic analysis of arabinoxylan containing cereal cell calls. J Agric Food Chem 59:6369–6375
18. Evers AD (1970) Development of endosperm of wheat. Ann Bot London 34:547–555
19. Finch-Savage WE, Leubner-Metzger G (2006) Seed dormancy and the control of germination. New Phytol 171:501–523
20. Fincher GB, Stone BA (2004) Chemistry of non-starch polysaccharides from cereal grains. In: Wrigley C, Corke H, Walker CE (eds) Encyclopedia of Grain Science. vol 1. ElsevierAcademic Press, Oxford, pp 206–223
21. Fineran BA, Wild DJC, Ingerfeld M (1982) Initial wall formation in the endosperm of wheat, Triticum aestivum—a re-evaluation. Can J Bot 60:1776–1795
22. Gao XP, Francis D, Ormrod JC, Bennett MD (1992) Changes in cell number and cell division activity during endosperm development in allohexaploid wheat, Triticum aestivum. J Exp Bot 43:1603–1609
23. Guillon F, Tranquet O, Quillien L, Utille JP, 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
24. Hay JO, Spanswick RM (2006) Mechanical and enzymatic separation of ripening rice (Oryza sativa L.) caryopsis tissues. Seed Sci Res 16:223–227
25. He JB, Penson S, Powers SJ, Hawes C, Shewry PR, Tosi P (2013) Spatial patterns of gluten protein and polymer distribution in wheat grain. J Agric Food Chem 61:6207–6215
26. Hesselman K, Elwinger K, Nilsson M, Thomke S (1981) The effect of beta-glucanase supplementation, stage of ripeness, and storage treatment of barley in diets fed to broiler chickens. Poultry Sci 60:2664–2671
27. Hoshikawa K (1973) Morphogenesis of endosperm tissue in rice. Jpn Agric Res Quart 7:153–159
28. Jones L, Seymour GB, Knox JP (1997) Localization of pectic galactan in tomato cell walls using a monoclonal antibody specific to (1→4)-beta-d-galactan. Plant Physiol 113:1405–1412
29. Juliano BO (1985) Cooperative tests on cooking properties of milled rice. CFW 30:651–656
30. Knox JP, Linstead PJ, King J, Cooper C, Roberts K (1990) Pectin esterification is spatially regulated both within cell walls and between developing tissues of root apices. Planta 181:512–521
31. Kozlova LV, Ageeva MV, Ibragimova NN, Gorshkova TA (2014) Arrangement of mixed-linkage glucan and glucuronoarabinoxylan in the cell walls of growing maize roots. Ann Bot 114:1135–1145
32. Lai VMF, Lu S, He WH, Chen HH (2007) Non-starch polysaccharide compositions of rice grains with respect to rice variety and degree of milling. Food Chem 101:1205–1210
33. Lazaridou A, Biliaderis CG (2007) Molecular aspects of cereal beta-glucan functionality: physical properties, technological applications and physiological effects. J Cereal Sci 46:101–118
34. Lee KJD, Sakata Y, Mau SL, Pettolino F, Bacic A, Quatrano RS, Knight CD, Knox JP (2005) Arabinogalactan proteins are required for apical cell extension in the moss Physcomitrella patens. Plant Cell 17:3051–3065
35. 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)-beta-d-glucan biosynthesis in barley. Plant Mol Biol 53:213–225
36. Marcus SE, Blake AW, Benians TAS, Lee KJD, Poyser C, Donaldson L, Leroux O, Rogowski A, Petersen HL, Boraston A, Gilbert HJ, Willats WGT, Knox JP (2010) Restricted access of proteins to mannan polysaccharides in intact plant cell walls. Plant J 64:191–203
37. Mares DJ, Stone BA (1973) Studies on wheat endosperm. 1. Chemical composition and ultrastructure of cell walls. Aust J Biol Sci 26:793–812
38. Mares DJ, Norstog K, Stone BA (1975) Early stages in development of wheat endosperm. 1. Change from free nuclear to cellular endosperm. Aust J Bot 23:311–326
39. McCartney L, Steele-King CG, Jordan E, Knox JP (2003) Cell wall pectic (1→4)-beta-d-galactan marks the acceleration of cell elongation in the Arabidopsis seedling root meristem. Plant J 33:447–454
40. McCartney L, Marcus SE, Knox JP (2005) Monoclonal antibodies to plant cell wall xylans and arabinoxylans. J Histochem Cytochem 53:543–546
41. Meikle PJ, Bonig I, Hoogenraad NJ, Clarke AE, Stone BA (1991) The location of (1-]3)-beta-glucans in the walls of pollen tubes of Nicotiana alata using a (1-]3)-beta-glucan-specific monoclonal antibody. Planta 185:1–8
42. Meikle PJ, Hoogenraad NJ, Bonig I, Clarke AE, Stone BA (1994) A (1-]3,1-]4)-beta-glucan-specific monoclonal-antibody and its use in the quantitation and immunocyto-chemical location of (1-]3,1-]4)-beta-glucans. Plant J 5:1–9
43. Moore JP, Farrant JM, Driouich A (2008) A role for pectin-associated arabinans in maintaining the flexibility of the plant cell wall during water deficit stress. Plant Signal Behav 3:102–104
44. Morrison IN, Obrien TP (1976) Cytokinesis in developing wheat-grain—division with and without a phragmoplast. Planta 130:57–67
45. Olsen OA (2001) Endosperm development: cellularization and cell fate specification. Annu Rev Plant Phys Plant Mol Biol 52:233–267
46. Olsen OA, Lemmon B, Brown R (1998) A model for aleurone development. Trends Plant Sci 3:168–169
47. Oparka KJ, Gates P (1981a) Transport of assimilates in the developing caryopsis of rice (Oryza sativa L)—the pathways of water and assimilated carbon. Planta 152:388–396
48. Oparka KJ, Gates P (1981b) Transport of assimilates in the developing caryopsis of rice (Oryza sativa L.)—ultrastructure of the pericarp vascular bundle and its connections with the aleurone layer. Planta 151:561–573
49. Oparka KJ, Gates P (1984) Sink anatomy in relation to solute movement in rice (Oryza sativa L.)—a summary of findings. Plant Growth Regul 2:297–307
50. Pedersen HL, Fangel JU, McCleary B, Ruzanski C, Rydahl MG, Ralet MC, Farkas V, von Schantz L, Marcus SE, Andersen MCF, Field R, Ohlin M, Knox JP, Clausen MH, Willats WGT (2012) Versatile high resolution oligosaccharide microarrays for plant glycobiology and cell wall research. J Biol Chem 287:39429–39438
51. Pellny TK, Lovegrove A, Freeman J, Tosi P, Love CG, Knox JP, Shewry PR, Mitchell RAC (2012) Cell walls of developing wheat starchy endosperm: comparison of composition and RNA-Seq transcriptome. Plant Physiol 158:612–627
52. Philippe S, Robert P, Barron C, Saulnier L, Guillon F (2006a) Deposition of cell wall polysaccharides in wheat endosperm during grain development—Fourier transform-infrared microspectroscopy study. J Agric Food Chem 54:2303–2308
53. Philippe S, Saulnier L, Guillon F (2006b) Arabinoxylan and (1 → 3), (1 → 4)-beta-glucan deposition in cell walls during wheat endosperm development. Planta 224:449–461
54. Piot O, Autran JC, Manfait M (2001) Investigation by confocal Raman microspectroscopy of the molecular factors responsible for grain cohesion in the Triticum aestivum bread wheat. Role of the cell walls in the starchy endosperm. J Cereal Sci 34:191–205
55. Ralet MC, Tranquet O, Poulain D, Moise A, Guillon F (2010) Monoclonal antibodies to rhamnogalacturonan-Ibackbone. Planta 231:1373–1383
56. Robert P, Jamme F, Barron C, Bouchet B, Saulnier L, Dumas P, Guillon F (2011) Change in wall composition of transfer and aleurone cells during wheat grain development. Planta 233:393–406
57. Sabelli PA, Larkins BA (2009) The development of endosperm in grasses. Plant Physiol 149:14–26
58. Scheller HV, Ulvskov P (2010) Hemicelluloses. Annu Rev Plant Biol 61:263–289
59. Shewry PR, Mitchell RAC, Tosi P, Wan YF, Underwood C, Lovegrove A, Freeman J, Toole GA, Mills ENC, Ward JL (2012) An integrated study of grain development of wheat (cv. Hereward). J Cereal Sci 56:21–30
60. Shibuya N (1989) Comparative studies on the cell wall polymers obtained from different parts of rice grains. ACS Symp Ser 399:333–344
61. Shibuya N, Nakane R (1984) Pectic polysaccharides of rice endosperm cell walls. Phytochemistry 23:1425–1429
62. 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
63. Shibuya N, Nakane R, Yasui A, Tanaka K, Iwasaki T (1985) Comparative studies on cell wall preparations from rice bran, germ, and endosperm. Cereal Chem 62:252–258
64. Threapleton DE, Greenwood DC, Evans CEL, Cleghorn CL, Nykjaer C, Woodhead C, Cade JE, Gale CP, Burley VJ (2013) Dietary fiber intake and risk of first stroke a systematic review and meta-analysis. Stroke 44:1360–1368
65. Toole GA, Barron C, Le Gall G, Colquhoun IJ, Shewry PR, Mills ENC (2009) Remodelling of arabinoxylan in wheat (Triticum aestivum) endosperm cell walls during grain filling. Planta 229:667–680
66. Toole GA, Le Gall G, Colquhoun IJ, Nemeth C, Saulnier L, Lovegrove A, Pellny T, Wilkinson MD, Freeman J, Mitchell RAC, Mills ENC, Shewry PR (2010) Temporal and spatial changes in cell wall composition in developing grains of w heat cv. Hereward. Planta 232:677–689
67. Toole GA, Le Gall G, Colquhoun IJ, Johnson P, Bedo Z, Saulnier L, Shewry PR, Mills ENC (2011) Spectroscopic analysis of diversity of arabinoxylan structures in endosperm cell walls of wheat cultivars (Triticum aestivum) in the HEALTHGRAIN diversity collection. J Agric Food Chem 59:7075–7082
68. Tosi P, D’Ovidio R, Napier JA, Bekes F, Shewry PR (2004) Expression of epitope-tagged LMW glutenin subunits in the starchy endosperm of transgenic wheat and their incorporation into glutenin polymers. Theor Appl Genet 108:468–476
69. Verhertbruggen Y, Marcus SE, Haeger A, Ordaz-Ortiz JJ, Knox JP (2009) An extended set of monoclonal antibodies to pectic homogalacturonan. Carbohydr Res 344:1858–1862
70. Verma DPS, Hong ZL (2001) Plant callose synthase complexes. Plant Mol Biol 47:693–701
71. Wang HL, Patrick JW, Offler CE, Wardlaw IF (1993) A novel experimental system for studies of photosynthate transfer in the developing wheat grain. J Exp Bot 44:1177–1184
72. Wang HL, Offler CE, Patrick JW, Ugalde TD (1994) The cellular pathway of photosynthate transfer in the developing wheat-grain. 1. Delineation of a potential transfer pathway using fluorescent dyes. Plant Cell Environ 17:257–266
73. Willats WGT, Marcus SE, Knox JP (1998) Generation of a monoclonal antibody specific to (1-5)-alpha-L-arabinan. Carbohydr Res 308:149–152
74. Wilson SM, Burton RA, Doblin MS, Stone BA, Newbigin EJ, Fincher GB, Bacic A (2006) Temporal and spatial appearance of wall polysaccharides during cellularization of barley (Hordeum vulgare) endosperm. Planta 224:655–667
75. Wilson SM, Burton RA, Collins HM, Doblin MS, Pettolino FA, Shirley N, Fincher GB, Bacic A (2012) Pattern of deposition of cell wall polysaccharides and transcript abundance of related cell wall synthesis genes during differentiation in barley endosperm. Plant Physiol 159:655–670
76. Zhou Q, Rutland MW, Teeri TT, Brumer H (2007) Xyloglucan in cellulose modification. Cellulose 14:625–641