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Front Plant Sci. 2021 Sep 23;12:737690. doi: 10.3389/fpls.2021.737690. eCollection 2021.

Xylan Is Critical for Proper Bundling and Alignment of Cellulose Microfibrils in Plant Secondary Cell Walls.

Frontiers in plant science

Jacob D Crowe, Pengchao Hao, Sivakumar Pattathil, Henry Pan, Shi-You Ding, David B Hodge, Jacob Krüger Jensen

Affiliations

  1. Department of Chemical Engineering & Materials Science, Michigan State University, East Lansing, MI, United States.
  2. Department of Chemistry, Michigan State University, East Lansing, MI, United States.
  3. Complex Carbohydrate Research Center, The University of Georgia, Athens, GA, United States.
  4. Department of Chemical Engineering, University of Texas, Austin, TX, United States.
  5. Department of Plant Biology, Michigan State University, East Lansing, MI, United States.
  6. Department of Energy Great Lakes Bioenergy Research Center, Michigan State University, East Lansing, MI, United States.
  7. Department of Chemical & Biological Engineering, Montana State University, Bozeman, MT, United States.
  8. Section for Plant Glycobiology, Department of Plant and Environmental Sciences, University of Copenhagen, Copenhagen, Denmark.

PMID: 34630488 PMCID: PMC8495263 DOI: 10.3389/fpls.2021.737690

Abstract

Plant biomass represents an abundant and increasingly important natural resource and it mainly consists of a number of cell types that have undergone extensive secondary cell wall (SCW) formation. These cell types are abundant in the stems of Arabidopsis, a well-studied model system for hardwood, the wood of eudicot plants. The main constituents of hardwood include cellulose, lignin, and xylan, the latter in the form of glucuronoxylan (GX). The binding of GX to cellulose in the eudicot SCW represents one of the best-understood molecular interactions within plant cell walls. The evenly spaced acetylation and 4-O-methyl glucuronic acid (MeGlcA) substitutions of the xylan polymer backbone facilitates binding in a linear two-fold screw conformation to the hydrophilic side of cellulose and signifies a high level of molecular specificity. However, the wider implications of GX-cellulose interactions for cellulose network formation and SCW architecture have remained less explored. In this study, we seek to expand our knowledge on this by characterizing the cellulose microfibril organization in three well-characterized GX mutants. The selected mutants display a range of GX deficiency from mild to severe, with findings indicating even the weakest mutant having significant perturbations of the cellulose network, as visualized by both scanning electron microscopy (SEM) and atomic force microscopy (AFM). We show by image analysis that microfibril width is increased by as much as three times in the severe mutants compared to the wild type and that the degree of directional dispersion of the fibrils is approximately doubled in all the three mutants. Further, we find that these changes correlate with both altered nanomechanical properties of the SCW, as observed by AFM, and with increases in enzymatic hydrolysis. Results from this study indicate the critical role that normal GX composition has on cellulose bundle formation and cellulose organization as a whole within the SCWs.

Copyright © 2021 Crowe, Hao, Pattathil, Pan, Ding, Hodge and Jensen.

Keywords: atomic force micorscopy (AFM); cell wall mechanical properties; cellulose arrangement; cellulose deposition; glucuronoxylan; irregular xylan mutants (irx); secondary cell wall (SCW); xylan (hemicellulose)

Conflict of interest statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

References

  1. Biotechnol Biofuels. 2012 Nov 26;5(1):84 - PubMed
  2. Int J Biol Macromol. 1993 Apr;15(2):109-12 - PubMed
  3. Plant Physiol. 2016 May;171(1):93-109 - PubMed
  4. Trends Plant Sci. 2019 May;24(5):402-412 - PubMed
  5. New Phytol. 2018 Jul;219(1):230-245 - PubMed
  6. Proc Natl Acad Sci U S A. 2018 Jun 19;115(25):6506-6511 - PubMed
  7. Curr Opin Biotechnol. 2019 Apr;56:97-104 - PubMed
  8. Plant J. 2007 Dec;52(6):1154-68 - PubMed
  9. J Struct Biol. 2020 Aug 1;211(2):107532 - PubMed
  10. Mater Sci Eng C Mater Biol Appl. 2017 Jan 1;70(Pt 1):207-215 - PubMed
  11. Plant J. 2008 May;54(4):559-68 - PubMed
  12. J Vis Exp. 2010 Mar 11;(37): - PubMed
  13. Methods Mol Biol. 2012;908:61-72 - PubMed
  14. Plant J. 2011 May;66(3):401-13 - PubMed
  15. Annu Rev Cell Dev Biol. 2006;22:53-78 - PubMed
  16. New Phytol. 2008;178(2):239-252 - PubMed
  17. Curr Biol. 2020 Mar 9;30(5):941-947.e2 - PubMed
  18. Plant J. 2014 Oct;80(2):207-15 - PubMed
  19. Glycobiology. 2012 Mar;22(3):439-51 - PubMed
  20. Biomacromolecules. 2008 Mar;9(3):1022-6 - PubMed
  21. C R Biol. 2004 Sep-Oct;327(9-10):785-90 - PubMed
  22. Plant Cell. 2013 Jan;25(1):270-87 - PubMed
  23. J Cell Biol. 1982 Jul;94(1):64-9 - PubMed
  24. Front Plant Sci. 2012 Aug 22;3:204 - PubMed
  25. Glycobiology. 2014 Jun;24(6):494-506 - PubMed
  26. Plant Signal Behav. 2014;9(1):e27809 - PubMed
  27. Biotechnol Biofuels. 2017 Nov 30;10:286 - PubMed
  28. Plant J. 2011 May;66(3):387-400 - PubMed
  29. Plant Physiol. 2012 Aug;159(4):1408-17 - PubMed
  30. Plant Cell. 2005 Aug;17(8):2281-95 - PubMed
  31. Philos Trans A Math Phys Eng Sci. 2018 Feb 13;376(2112): - PubMed
  32. Plant Cell. 2007 Feb;19(2):549-63 - PubMed
  33. Ann Bot. 2018 May 11;121(6):1107-1125 - PubMed
  34. Proc Natl Acad Sci U S A. 2012 Aug 28;109(35):14253-8 - PubMed
  35. Carbohydr Polym. 2021 Oct 15;270:118364 - PubMed
  36. Front Plant Sci. 2019 Oct 23;10:1398 - PubMed
  37. Curr Opin Plant Biol. 2008 Jun;11(3):258-65 - PubMed
  38. ACS Nano. 2020 Jan 28;14(1):724-735 - PubMed
  39. Biotechnol Biofuels. 2015 Mar 12;8:41 - PubMed
  40. Nat Biotechnol. 2018 Mar;36(3):249-257 - PubMed
  41. Plant J. 2014 Aug;79(3):492-506 - PubMed
  42. Bioresour Technol. 2017 Dec;245(Pt A):242-249 - PubMed
  43. Plant Physiol. 2010 Jun;153(2):542-54 - PubMed
  44. Nat Plants. 2017 Nov;3(11):859-865 - PubMed
  45. Science. 2012 Nov 23;338(6110):1055-60 - PubMed
  46. New Phytol. 2018 May;218(3):1049-1060 - PubMed
  47. Plant Physiol. 2016 Aug;171(4):2418-31 - PubMed
  48. Plant Physiol. 2010 Jun;153(2):526-41 - PubMed
  49. Plant Physiol. 2010 Sep;154(1):121-33 - PubMed
  50. Proc Natl Acad Sci U S A. 2016 Oct 4;113(40):11348-11353 - PubMed
  51. Biochem Soc Trans. 2016 Feb;44(1):74-8 - PubMed
  52. Biomacromolecules. 2017 Apr 10;18(4):1311-1321 - PubMed
  53. Phys Chem Chem Phys. 2013 Jun 7;15(21):8429-40 - PubMed
  54. Curr Opin Plant Biol. 2014 Dec;22:122-131 - PubMed
  55. Plant Cell Physiol. 2009 Jun;50(6):1099-115 - PubMed
  56. Plant Cell Physiol. 2009 Jun;50(6):1075-89 - PubMed
  57. Plant Physiol. 2010 Feb;152(2):787-96 - PubMed
  58. New Phytol. 2015 Jan;205(2):666-81 - PubMed
  59. Nat Commun. 2016 Dec 21;7:13902 - PubMed
  60. Plant Cell Physiol. 2016 Aug;57(8):1707-19 - PubMed
  61. Plant J. 2009 Feb;57(4):718-31 - PubMed
  62. Plant J. 2009 Feb;57(4):732-46 - PubMed
  63. Plant J. 2013 May;74(3):423-34 - PubMed
  64. Sci Rep. 2019 Mar 7;9(1):3869 - PubMed
  65. Plant J. 2015 Aug;83(3):413-26 - PubMed
  66. Biotechnol Biofuels. 2010 May 24;3:10 - PubMed
  67. Front Plant Sci. 2020 Apr 24;11:479 - PubMed
  68. PLoS One. 2014 Aug 13;9(8):e105014 - PubMed
  69. New Phytol. 2019 Mar;221(4):1703-1723 - PubMed
  70. Plant Physiol. 2016 Jan;170(1):234-49 - PubMed
  71. Biotechnol Biofuels. 2019 May 6;12:109 - PubMed
  72. Plant Physiol. 2013 Dec;163(4):1558-67 - PubMed
  73. Plant J. 2014 Oct;80(2):197-206 - PubMed
  74. Plant J. 2016 Jan;85(2):179-92 - PubMed
  75. Plant Cell Physiol. 2007 Dec;48(12):1659-72 - PubMed
  76. J Vis Exp. 2010 Mar 12;(37): - PubMed
  77. Mol Plant. 2013 Mar;6(2):570-3 - PubMed

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