Zoom in on Ca²⁺pattern and ion flux dynamics to decode spatial and temporal regulation of cotton fiber growth

Abstract

Cotton fibers are single-celled trichomes initiated from ovule epidermis prior to anthesis. Thereafter, the fibers undergo rapid elongation for 20 d before switching to intensive cell wall cellulose synthesis. The final length attained determines fiber yield and quality. As such, cotton fiber represents an excellent single cell model to study regulation of cell growth and differentiation, with significant agronomical implications. One major unresolved question is whether fiber elongation follows a diffusive or a tip growth pattern. We addressed this issue by using cell biology and electrophysiological approaches. Confocal imaging of Ca2+ binding dye, fluo-3 acetoxymethyl (Fluo-3), and in situ microelectrode ion flux measurement revealed that cytosolic Ca2+ was evenly distributed along the elongating fiber cells with Ca2+ and H+ fluxes oscillating from apical to basal regions of the elongating fibers. These findings demonstrate that, contrary to growing pollen tubes or root hairs, cotton fiber growth follows a diffusive, but not the tip growth, pattern. Further analyses showed that the elongating fibers exhibited substantial net H+ efflux, indicating a strong activity of the plasma membrane H+-ATPase required for energy dependent solute uptake. Interestingly, the growing cotton fibers were responding to H2O2 treatment, know to promote fiber elongation, by a massive increase in the net Ca2+ and H+ efflux in both tip and basal zones, while non-growing cells lacked this ability. These observations suggest that desensitization of the cell and a loss of its ability to respond to H2O2 may be causally related to the termination of the cotton fiber elongation.

GhRabA4c coordinates cell elongation via regulating actin filament–dependent vesicle transport

“…One possible explanation for the functional differences between GhRabA4c and Arabidopsis RabA GTPases in regulating cell wall component deposition is that the biological functions of RabA GTPases may have evolved to adapt the growth characteristics of cotton fibers. As described previously, cotton fibers elongate rapidly in a tip-biased diffuse growth manner ( Yu et al, 2019 ) or diffuse growth manner ( Yang et al, 2021 Preprint ), which is different from the tip growth manner in pollen tubes and root hairs. Thus, it is likely that the function of a RabA GTPase, originally responsible for only one cell wall component for tip growth cells, has evolved to participate in the deposition of multiple cell wall components simultaneously in cotton fibers.…”

“…However, the potential roles of RabA GTPase in diffuse cell growth have never been reported in plants. In this context, several lines of observations show that cotton fibers elongate mainly via diffuse growth mode ( Seagull, 1990 ; Tiwari & Wilkins, 1995 ; Ruan, 2007 ; Yang et al, 2021 Preprint ). In this study, we examined the role of RabA GTPase in cell growth by using cotton fiber as a model.…”