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Apical pollen tube wall curvature correlates with growth and indicates localized changes in the yielding of the cell wall

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Abstract

The shape of the apical region of lily pollen tube changes rhythmically as the growth rate of the tube oscillates becoming alternately more prolate then back to oblate. We quantified shape change by calculating the curvature of the cross-sectional edge of the pollen tube tip and cross-correlating curvature changes with growth rate. The apical region takes the form of a partial elliptical spheroid, with variation in the length and location of the minor axis. During oscillation curvature profiles show a sharp increase in curvature at the “shoulders” of the apex when oblate, 4–7 μm from the flatter central zone. As the tip becomes more prolate, the “shoulders” decrease rapidly in curvature and move towards the growth axis as curvature at the tip increases. We understand curvature changes to represent differential changes in local wall expansion rates, driven by uniform turgor pressure and mediated by changes in wall polysaccharides. To become more oblate, the tip region must become less extensible than the “shoulder” region. And, as the tip becomes more prolate, the increased curvature must be due to increased local expansion. We found that changes in the growth velocity of the “shoulders” of the cell measured as the progress of the cell edge along the growth axis are cyclically out of phase with growth velocity at the tip such that the shoulder regions lag for part of the oscillation cycle, then “catch up” as the growth rate at the tip reaches a maximum and begins to decline. In this way the cell becomes oblate. Cell shape and growth rate oscillate in concert and are functionally related. Spatial change in edge growth rate points to important cellular locations for further investigation of vesicle movement and exocytosis, calcium gradients, and actin dynamics in lily pollen tubes.

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All data and images are available on request to the corresponding author.

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R scripts used during image and data analysis are available from the corresponding author.

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Funding

This work was supported by the research grant MCB-0847876, from the National Science Foundation to PKH and by funds from the University of Massachusetts Research Trust Fund also to PKH.

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All authors contributed to the study conception and design. Material preparation, data collection, and analysis were performed by Grace Rosen and Lawrence Winship. The first draft of the manuscript was written by Grace Rosen as her senior thesis at Hampshire College, and all authors commented on previous versions of the manuscript. Peter Hepler and Lawrence Winship edited, read, and approved the final manuscript.

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Correspondence to Lawrence J. Winship.

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The authors declare no competing interests.

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Handling Editor: Andreas Holzinger.

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This manuscript is an invited submission to a special issue entitled “Ultrastructure of Plant Cells,” edited by Andreas Holzinger, dedicated as a memorial to Dr. Ursula Lütz-Meindl.

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Winship, L.J., Rosen, G.A. & Hepler, P.K. Apical pollen tube wall curvature correlates with growth and indicates localized changes in the yielding of the cell wall. Protoplasma 258, 1347–1358 (2021). https://doi.org/10.1007/s00709-021-01694-2

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  • DOI: https://doi.org/10.1007/s00709-021-01694-2

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