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Changes in the orientations of cellulose microfibrils during the development of collenchyma cell walls of celery (Apium graveolens L.)

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Abstract

Main conclusion

During development, cellulose microfibrils in collenchyma walls become increasingly longitudinal, as determined by small-angle X-ray scattering, despite the walls maintaining a fine structure indicative of a crossed-polylamellate structure.

Abstract

Collenchyma cells have thickened primary cell walls and provide mechanical support during plant growth. During their development, these cells elongate and their walls thicken considerably. We used microscopy and synchrotron small-angle X-ray scattering to study changes in the orientations of cellulose microfibrils that occur during development in the walls of collenchyma cells present in peripheral strands in celery (Apium graveolens) petioles. Transmission electron microscopy showed that the walls consisted of many lamellae (polylamellate), with lamellae containing longitudinally oriented cellulose microfibrils alternating with microfibrils oriented at higher angles. The lamellae containing longitudinally oriented microfibrils predominated at later stages of development. Nevertheless, transmission electron microscopy of specially stained, oblique sections provided evidence that the cellulose microfibrils were ordered throughout development as crossed-polylamellate structures. These results are consistent with our synchrotron small-angle X-ray scattering results that showed the cellulose microfibrils become oriented increasingly longitudinally during development. Some passive reorientation of cellulose microfibrils may occur during development, but extensive reorientation throughout the wall would destroy ordered structures. Atomic force microscopy and field emission scanning electron microscopy were used to determine the orientations of newly deposited cellulose microfibrils. These were found to vary widely among different cells, which could be consistent with the formation of crossed-polylamellate structures. These newly deposited cellulose microfibrils are deposited in a layer of pectic polysaccharides that lies immediately outside the plasma membrane. Overall, our results show that during development of collenchyma walls, the cellulose microfibrils become increasingly longitudinal in orientation, yet organized, crossed-polylamellate structures are maintained.

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Abbreviations

CAPS:

3-(Cyclohexylamino)-1-propanesulfonic acid

CM-AFM:

Contact mode atomic force microscopy

DTT:

Dithiothreitol

FESEM:

Field emission scanning electron microscopy

FTIR:

Fourier-transform infrared

HEPES:

4-(2-Hydroxyethyl)-1-piperazineethanesulfonic acid

HG:

Homogalacturonan

PATAg:

Periodic acid–thiocarbohydrazide–silver proteinate

RG-I:

Rhamnogalacturonan-I

SAXS:

Small-angle X-ray scattering

TEM:

Transmission electron microscopy

VPSEM:

Variable pressure scanning electron microscopy

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Acknowledgements

We thank Stan Clark for providing the celery, Dr Yiran An for technical assistance with the AFM, Dr Adrian Turner for help with the TEM, and Associate Professor Guy Cox of the University of Sydney for helpful discussions. We gratefully acknowledge funding from the University of Auckland.

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Correspondence to Philip J. Harris.

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Chen, D., Melton, L.D., McGillivray, D.J. et al. Changes in the orientations of cellulose microfibrils during the development of collenchyma cell walls of celery (Apium graveolens L.). Planta 250, 1819–1832 (2019). https://doi.org/10.1007/s00425-019-03262-8

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