A mechanohydraulic model supports a role for plasmodesmata in cotton fiber elongation

Abstract

AbstractPlant cell growth depends on turgor pressure, the cell hydrodynamic pressure, which drives expansion of the extracellular matrix (the cell wall). Turgor pressure regulation depends on several physical, chemical and biological factors, including: vacuolar invertases, which modulate osmotic pressure of the cell, aquaporins, which determine the permeability of the plasma membrane, cell wall remodeling factors, which determine cell wall extensibility (inverse of effective viscosity), and plasmodesmata, which are membrane-lined channels that allow free movement of water and solutes between cytoplasms of neighbouring cells, like gap junctions in animals. Plasmodesmata permeability varies during plant development and experimental studies have correlated changes in the permeability of plasmodesmal channels to turgor pressure variations. Here we study the role of plasmodesmal permeability in cotton fiber growth, a type of cell that increase in length by at least 3 orders of magnitude in a few weeks. We incorporated plasmodesma-dependent movement of water and solutes into a classical model of plant cell expansion. We performed a sensitivity analysis to changes in values of model parameters and found that plasmodesmal permeability is among the most important factors for building up turgor pressure and expanding cotton fibers. Moreover, we found that non-monotonic behaviors of turgor pressure that have been reported previously in cotton fibers cannot be recovered without accounting for dynamic changes of the parameters used in the model. Altogether, our results suggest an important role for plasmodesmal permeability in the regulation of turgor pressure.Significance StatementThe cotton fiber is among the plant cells with the highest growth rates. In cultivars, a single fiber cell generally reaches a few centimeters in length. How such size is achieved is still poorly understood. In order to tackle this question, we built a comprehensive mathematical model of fiber elongation, considering cell mechanics and water entry into the cell. Model predictions agree with experimental observations, provided that we take into account active opening and closure of plasmodesmata, the sub-micrometric channels that connect the fiber with neighboring cells. Because cotton fiber length is a key factor for yarn quality, our work may help understanding the mechanisms behind an important agronomic trait.