Spatial organization of cellulose microfibrils and matrix polysaccharides in primary plant cell walls as imaged by multichannel atomic force microscopy

Tian Zhang, Yunzhen Zheng, Daniel J. Cosgrove

Research output: Contribution to journalArticle

84 Scopus citations

Abstract

We used atomic force microscopy (AFM), complemented with electron microscopy, to characterize the nanoscale and mesoscale structure of the outer (periclinal) cell wall of onion scale epidermis - a model system for relating wall structure to cell wall mechanics. The epidermal wall contains ~100 lamellae, each ~40 nm thick, containing 3.5-nm wide cellulose microfibrils oriented in a common direction within a lamella but varying by ~30 to 90° between adjacent lamellae. The wall thus has a crossed polylamellate, not helicoidal, wall structure. Montages of high-resolution AFM images of the newly deposited wall surface showed that single microfibrils merge into and out of short regions of microfibril bundles, thereby forming a reticulated network. Microfibril direction within a lamella did not change gradually or abruptly across the whole face of the cell, indicating continuity of the lamella across the outer wall. A layer of pectin at the wall surface obscured the underlying cellulose microfibrils when imaged by FESEM, but not by AFM. The AFM thus preferentially detects cellulose microfibrils by probing through the soft matrix in these hydrated walls. AFM-based nanomechanical maps revealed significant heterogeneity in cell wall stiffness and adhesiveness at the nm scale. By color coding and merging these maps, the spatial distribution of soft and rigid matrix polymers could be visualized in the context of the stiffer microfibrils. Without chemical extraction and dehydration, our results provide multiscale structural details of the primary cell wall in its near-native state, with implications for microfibrils motions in different lamellae during uniaxial and biaxial extensions. Significance Statement The outer (periclinal) cell wall of the onion scale epidermis is a useful model for relating wall structure to cell wall mechanics and spectroscopy. Here we use advanced atomic force microscopy to uncover the nanoscale organization of cellulose microfibrils and matrix components within individual lamellae as well as the mesoscale organization of the ~100 lamellae comprising the wall. These details provide a foundation for multiscale models of the mechanics and growth of primary cell walls.

Original languageEnglish (US)
Pages (from-to)179-192
Number of pages14
JournalPlant Journal
Volume85
Issue number2
DOIs
StatePublished - Jan 1 2016

    Fingerprint

All Science Journal Classification (ASJC) codes

  • Genetics
  • Plant Science
  • Cell Biology

Cite this