New insights into the structural and spatial variability of cell-wall polysaccharides during wheat grain development, as revealed through MALDI mass spectrometry imaging

Journal of Experimental Botany

Volumn 65, Issue 8, 2014, Pages 2079-2091

  Veličković, Dušan ^a   Ropartz, David ^a   Guillon, Fabienne ^a   Saulnier, Luc ^a   Rogniaux, Hélène ^a  

^a INRA   (France)

Author keywords

Acetylated arabinoxylan; beta glucans; cell wall; imaging; in situ digestion; mass spectrometry; wheat

Indexed keywords

ARABINOXYLAN; BETA GLUCAN; XYLAN;

CELL WALL; CHEMISTRY; ENDOSPERM; GROWTH, DEVELOPMENT AND AGING; MASS SPECTROMETRY; METABOLISM; WHEAT;

BETA-GLUCANS; CELL WALL; ENDOSPERM; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; TRITICUM; XYLANS;

EID: 84898989569     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/eru065     Document Type: Article

References (61)

1. Angel PM, Caprioli RM. 2013. Matrix-Assisted laser desorption ionization imaging mass spectrometry: In situ molecular mapping. Biochemistry 52, 3818-3828
2. Bacon JSD, Gordon AH, Morris EJ. 1975. Acetyl groups in cell-wall preparations from higher plants. The Biochemical Journal 149, 485-487
3. Beaugrand J, Crônier D, Thieban P, Schreiber L, Debeire P, Chabbert B. 2004. Structure, chemical composition and xylanase degradation of external layers isolated from developing wheat grains. Journal of Agricultural and Food Chemistry 52, 7108-7117
4. Berrin JG, Juge N. 2008. Factors affecting xylanase functionality in the degradation of arabinoxylans. Biotechnology Letters 7, 1139-1150
5. Biely P, MacKenzie CR, Puls J, Schneider H. 1986. Cooperativity of esterases and xylanases in the enzymatic degradation of acetyl xylan. Nature Biotechnology 4, 731-733
6. Biely P, Puls J, Schneider H. 1985. Acetyl xylan esterases in fungal cellulolytic systems. FEBS Letters 186, 80-84
7. Biely P, VrŠanskα M, Tenkanen M, Kluepfel D. 1997. Endo-β-1,4-xylanase families: Differences in catalytic properties. Journal of Biotechology 57, 151-166
8. Burrell MM, Earnshaw CJ, Clench MR. 2007. Imaging matrix assisted laser desorption ionization mass spectrometry: A technique to map plant metabolites within tissues at high spatial resolution. Journal of Experimental Botany 58, 757-763
9. Choi SS, Ha SH. 2006. Characterization of ionized maltooligosaccharides by sodium cation in MALDI-TOFMS depending on the molecular size. Bulletin of the Korean Chemical Society 27, 1243-1245
10. Deininger SO, Cornett DS, Raape R, Becker M, Pineau C, Rauser S, Walch A, Wolsky E. 2011. Normalization in MALDI-TOF imaging datasets of proteins: Practical considerations. Analytical and Bioanalytical Chemistry 401, 167-181
11. Dervilly G, Saulnier L, Roger P, Thibault JF. 2000. Isolation of homogeneous fractions from wheat water-soluble arabinoxylans. Influence of the structure on their macromolecular characteristics. Journal of Agricultural and Food Chemistry 48, 270-278
12. Fauré R, Courtin CM, Delcour JA, et al., 2009. A brief and informationally rich naming system for oligosaccharide motifs of heteroxylans found in plant cell walls. Australian Journal of Chemistry 62, 533-537
13. Fincher GB, Stone BA. 1986. Cell walls and their components in cereal grain technology. In: Pomeranz Y, ed, Advances in cereal science and technology. St Paul, MN: American Association of Cereal Chemists, pp 207-295
14. Franceschi P, Dong Y, Strupat K, Vrhovsek U, Mattivi F. 2012. Combining intensity correlation analysis and MALDI imaging to study the distribution of flavonols and dihydrolchalcones in Golden Delicious apple. Journal of Experimental Botany 63, 1123-1133
15. Ghotra BS, Vasanthan T, Temelli F. 2008. Structural characterization of barley β-glucan extracted using a novel fractionation technique. Food Research International 41, 957-963
16. Gille S, de Souza A, Xiong G, Benz M, Cheng K, Schultink A, Reca IB, Pauly M. 2011. O-Acetylation of Arabidopsis hemicellulose xyloglucan requires AXY4 or AXY4L, proteins with TBL and DUF231 domain. The Plant Cell 23, 4041-4053
17. Goodwin RJA. 2012. Sample preparation for mass spectrometry imaging: Small mistakes can lead to big consequences. Journal of Proteomics 75, 4893-4911
18. Hamm G, Bonnel D, Legouffe R, Pamelard F, Deblos JM, Bouzom F, Stauber J. 2012. Quantitative mass spectrometry imaging of propranolol and olanzapine using tissue extinction calculation as normalization factor. Journal of Proteomics 75, 4952-4961
19. Harris PJ, Smith BG. 2006. Plant cell walls and cell-wall polysaccharides: Structures, properties and uses in food products. International Journal of Food Science and Technology 41, 129-143
20. Harvey DJ. 1993. Quantitative aspects of the matrix-Assisted laser desorption mass spectrometry of complex oligosaccharides. Rapid Communications in Mass Spectrometry 7, 614-619
21. Horn PJ, Korte AR, Neogi BP, Love E, Fuchs J, Strupat K, Borisjuk L, Shulaev V, Lee YJ, Chapman KD. 2012. Spatial mapping of lipids at cellular resolution in embryos of cotton. The Plant Cell 24, 622-636
22. Kabel MA, Van Den Borne H, Vincken JP, Voragen AGJ, Schols HA. 2007. Structural differences of xylans affect their interaction with cellulose. Carbohydrate Polymers 69, 94-105
23. Källback P, Shariatgorji M, Nilsson A, Andrén PE. 2012. Novel mass spectrometry imaging software assisting labeled normalization and quantification of drugs and neuropeptides directly in tissue sections. Journal of Proteomics 75, 4941-4951
24. Kaspar S, Peukert M, Svatos A, Matros A, Mock HP. 2011. MALDIimaging mass spectrometry-An emerging technique in plant biology. Proteomics 11, 1840-1850
25. Lazaridou A, Biliaderis CG. 2007. Molecular aspects of cereal β-glucan functionality: Physical properties, technological applications and physiological effects. Journal of Cereal Science 46, 101-118
26. Lee YJ, Perdian DC, Song Z, Yeung ES, Nikolau BJ. 2012. Use of mass spectrometry for imaging metabolites in plants. The Plant Journal 70, 81-95
27. Lequart C, Nuzillard JM, Kurek B, Debeire P. 1999. Hydrolysis of wheat bran and straw by an endoxylanase: Production and structural characterization of cinnamoyl-oligosaccharides. Carbohydrate Research 319, 102-111
28. Lunsford KA, Peter GF, Yost RA. 2011. Direct matrix-Assisted laser desorption/ionization mass spectrometric imaging of cellulose and hemicellulose in Populus tissue. Analytical Chemistry 83, 6722-6730
29. Nimesh S, Mohottalge S, Vincent R, Kumarathasan P. 2013. Current status and future perspectives of mass spectrometry imaging. International Journal of Molecular Sciences 14, 11277-11301
30. Obel N, Erben V, Schwarz T, KÜhnel S, Fodor A, Pauly M. 2009. Microanalysis of plant cell wall polysaccharides. Molecular Plant 2, 922-932
31. Obel N, Porchia AC, Scheller HV. 2002. Dynamic changes in cell wall polysaccharides during wheat seedling development. Phytochemistry 60, 603-610
32. Ordaz-Ortiz JJ, Devaux MF, Saulnier L. 2005. Classification of wheat varieties based on structural features of arabinoxylans as revealed by endoxylanase treatment of flour and grain. Journal of Agricultural and Food Chemistry 53, 8349-8356
33. Perdian DC, Lee YJ. 2010. Imaging MS methodology for more chemical information in less data acquisition time utilizing a hybrid linear ion traporbitrap mass spectrometer. Analytical Chemistry 82, 9393-9400
34. Philippe S, Barron C, Robert P, Devaux MF, Saulnier L, Guillon F. 2006c. Characterization using Raman microspectroscopy of arabinoxylans in the walls of different cell types during development of wheat endosperm. Journal of Agricultural and Food Chemistry 54, 5113-5119
35. Philippe S, Robert P, Barron C, Saulnier L, Guillon F. 2006b. Deposition of cell wall polysaccharides in wheat endosperm during grain development: Fourier transform-infrared microspectroscopy study. Journal of Agricultural and Food Chemistry 54, 2303-2308
36. Philippe S, Saulnier L, Guillon F. 2006a. Arabinoxylan and (1-3),(1-4)-β-glucan deposition in cell walls during wheat endosperm development. Planta 224, 449-461
37. Philippe S, Tranquet O, Utille JP, Saulnier L, Guillon F. 2007. Ferulic acid in walls of endosperm of mature and developing wheat. Planta 225, 1287-1299
38. Rhodes DI, Sadek M, Stone BA. 2002. Hydroxycinnamic acid in walls of wheat aleurone cells. Journal of Cereal Science 36, 67-81
39. 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
40. Robinson S, Warburton K, Seymour M, Clench M, Thomas-Oates J. 2007. Localization of water-soluble carbohydrates in wheat stems using imaging matrix-Assisted laser desorption ionization mass spectrometry. New Phytologist 173, 438-444
41. Ropartz D, Bodet PE, Przybylski C, Gonnet F, Daniel R, Fer M, Helbert W, Bertrand D, Rogniaux H. 2011. Performance evaluation on a wide set of matrix-Assisted laser desorption ionization matrices for the detection of oligosaccharides in a high-Throughput mass spectrometric screening of carbohydrate depolymerizing enzymes. Rapid Communications in Mass Spectrometry 25, 2059-2070
42. Saulnier L, Guillon F, Chateigner-Boutin AL. 2012. Cell wall deposition and metabolism in wheat grain. Journal of Cereal Science 56, 91-108
43. Saulnier L, Guillon F, Sado PE, Rouau X. 2007a. Plant cell wall polysaccharides in storage organs: Xylans (food applications). In: Kamerling J, Boons GJ, Lee Y, Suzuki A, Taniguchi N, Voragen AGJ, eds, Comprehensive glycoscience. Oxford: Elsevier Science, pp 653-689
44. Saulnier L, Robert P, Grintchenko M, Jamme F, Bouchet B, Guillon F. 2009. Wheat endosperm cell walls: Spatial heterogeneity of polysaccharide structure and composition using micro-scale enzymatic fingerprinting and FT-IR microspectroscopy. Journal of Cereal Science 50, 312-317
45. Saulnier L, Sado PE, Branlard G, Charmet G, Guillon F. 2007b. Wheat arabinoxylans: Exploiting variation in amount and composition to develop enhanced varieties. Journal of Cereal Science 46, 261-281
46. Shroff R, Vergara F, Muck A, SvatoŠ A, Gershenzon J. 2008. Nonuniform distribution of glucosinolates in Arabidopsis thaliana leaves has important consequences for plant defense. Proceedings of the National Academy of Sciences, USA 105, 6196-6201
47. Snovida IS, Perreault H. 2007. A 2,5-Dihydroxybenzoic acid/N, Ndimethylaniline matrix for the analysis of oligosaccharides by matrixassisted laser desorption/ionization mass spectrometry. Rapid Communications in Mass Spectrometry 21, 3711-3715
48. Snovida IS, Chen VC, Perreault H. 2006. Use of 2,5-Dihydroxybenzoic acid/aniline MALDI matrix for improved detection and on-Target derivatization of glycans: A preliminary report. Analytical Chemistry 78, 8561-8568
49. Sørensen HR, Pedersen S, Meyer AS. 2007. Characterization of solubilized arabinoxylo-oligosaccharides by MALDI-TOF MS analysis to unravel and direct enzyme catalyzed hydrolysis of insoluble wheat arabinoxylan. Enzyme and Microbial Technology 41, 103-110
50. Stoeckli M, Staab D, Schweitzer A. 2007. Compound and metabolite distribution measured by MALDI mass spectrometric imaging in wholebody tissue sections. International Journal of Mass Spectrometry 260, 195-202
51. Sugiura Y, Setou M. 2010. Planning the sample preparation. In: Setou M, ed, Imaging mass spectrometry. Tokyo: Springer. pp 11-30
52. Toole GA, Barron C, Le Gall G, Colquhoun IJ, Shewry PR, Mills ENC. 2009. Remodeling of arabinoxylan in wheat (Triticum aestivum) endosperm cell walls during grain filling. Planta 229, 667-680
53. Toole GA, Le Gall G, Colquhoun IJ, et al., 2010. Temporal and spatial changes in cell wall composition in developing grains of wheat cv. Hereward. Planta 232, 677-689
54. Toole GA, Le Gall G, Colquhoun IJ, Johnson P, Bedö 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. Journal of Agricultural and Food Chemistry 59, 7075-7082
55. Tosh SM, Brummer Y, Wood PJ, Wang Q, Weisz J. 2004. Evaluation of structure in the formation of gels by structurally diverse (1-3) (1-4)-β-glucans from four cereal and one lichen species. Carbohydrate Polymers 57, 249-259
56. Vardakou M, Katapodis P, Samiotaki M, Kekos D, Panayotou G, Christakopoulos P. 2003. Mode of action of family 10 and 11 endoxylanases on water-unextractable arabinoxylan. International Journal of Biological Macromolecules 33, 129-134
57. Vorwerk S, Somerville S, Somerville C. 2004. The role of plant cell wall polysaccharide composition in disease resistance. Trends in Plant Science 9, 203-209
58. Wood PJ. 2002. Relationships between solution properties of cereal β-glucans and physiological effects-A review. Trends in Food Science and Technology 13, 313-320
59. Wood PJ, Weisz J, Blackwell BA. 1991. Molecular characterization of cereal β-D-glucans. Structural analysis of oat β-D-glucan and rapid structural evaluation of β-D-glucans from different sources by highperformance liquid chromatography of oligosaccharides released by lichenase. Cereal Chemistry 68, 31-39
60. Ye H, Gemperline E, Venkateshwaran M, Chen R, Delaux PM, Howes-Podoli M, Ané JM, Li L. 2013. MALDI mass spectrometryassisted molecular imaging of metabolites during nitrogen fixation in the Medicago truncatula-Sinorhizobium meliloti symbiosis. The Plant Journal 75, 130-145
61. Zhang JH, Siika-Aho M, Tenkanen M, Viikari L. 2011. The role of acetyl xylan esterase in the solubilization of xylan and enzymatic hydrolysis of wheat straw and giant reed. Biotechnology for Biofuels 4, 60