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Abstract In plant cells, linkage between the cytoskeleton, plasma membrane, and cell wall is crucial for maintaining cell shape. In highly polarized pollen tubes, this coordination is especially important to allow rapid tip growth and successful fertilization. Class I formins contain cytoplasmic actin-nucleating formin homology domains as well as a proline-rich extracellular domain and are candidate coordination factors. Here, using Arabidopsis, we investigated the functional significance of the extracellular domain of two pollen-expressed class I formins: AtFH3, which does not have a polar localization, and AtFH5, which is limited to the growing tip region. We show that the extracellular domain of both is necessary for their function, and identify distinct O-glycans attached to these sequences, AtFH5 being hydroxyproline-arabinosylated and AtFH3 carrying arabinogalactan chains. Loss of hydroxyproline arabinosylation altered the plasma membrane localization of AtFH5 and disrupted actin cytoskeleton organization. Moreover, we show that O-glycans differentially affect lateral mobility in the plasma membrane. Together, our results support a model of protein sub-functionalization in which AtFH5 and AtFH3, restricted to specific plasma membrane domains by their extracellular domains and the glycans attached to them, organize distinct subarrays of actin during pollen tube elongation.
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Constrained Nonlinear and Mixed Effects Integral Differential Equation Models for Dynamic Cell Polarity Signaling
Polar cell growth is a process that couples the establishment of cell polarity with growth and is extremely important in the growth, development, and reproduction of eukaryotic organisms, such as pollen tube growth during plant fertilization and neuronal axon growth in animals. Pollen tube growth requires dynamic but polarized distribution and activation of a signaling protein named ROP1 to the plasma membrane via three processes: positive feedback and negative feedback regulation of ROP1 activation and its lateral diffusion along the plasma membrane. In this paper, we introduce a mechanistic integro-differential equation (IDE) along with constrained semiparametric regression to quantitatively describe the interplay among these three processes that lead to the polar distribution of active ROP1 at a steady state. Moreover, we introduce a population variability by a constrained nonlinear mixed model. Our analysis of ROP1 activity distributions from multiple pollen tubes revealed that the equilibrium between the positive and negative feedbacks for pollen tubes with similar shapes are remarkably stable, permitting us to infer an inherent quantitative relationship between the positive and negative feedback loops that defines the tip growth of pollen tubes and the polarity of tip growth.
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- Award ID(s):
- 1853698
- PAR ID:
- 10337796
- Date Published:
- Journal Name:
- Frontiers in Plant Science
- Volume:
- 13
- ISSN:
- 1664-462X
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.3389/fpls.2022.847671
