Rapid cell expansion and cellulose synthesis regulated by plasmodesmata and sugar: insights from the single-celled cotton fibre

Abstract

Abstract.Higher plants comprise mixtures of some 40 different cell types, and this often complicates the interpretation of data obtained at the tissue level. Studies for a given cell type may provide novel insights into the mechanisms underlying defined cellular and developmental processes. In this regard, the cotton fibre represents an excellent single-cell model to study the control of rapid cell elongation and cellulose synthesis. These single cells, initiated from the ovule epidermis at anthesis, typically elongate to ∼3-5 cm in the tetraploid species before they switch to intensive secondary cell wall cellulose synthesis. By maturity, more than 94% of fibre weight is cellulose. To unravel the mechanisms of fibre elongation and cellulose synthesis, two hypotheses have been examined: (a) that sucrose degradation and utilisation mediated by sucrose synthase (Sus) may play roles in fibre development and (b) that symplastic isolation of the fibre cells may be required for their rapid elongation. Reverse genetic and biochemical analyses have revealed the critical role that Sus plays in fibre initiation and early elongation. Late in development, plasma-membrane and cell wall association of Sus protein seems to be involved in rapid cellulose synthesis. Cell biology and gene expression studies showed a temporary closure of fibre plasmodesmata (PD), probably due to the deposition of callose, at the rapid phase of elongation. The duration of the PD closure correlates positively with the final fibre length attained. These data support the view that PD closure may be required for fibres to achieve extended elongation. The branching of PD towards the secondary cell wall stage is postulated to function as a molecule sieve for tight control of macromolecule trafficking into fibres to sustain intensive cellulose synthesis.

Evidence That High Activity of Vacuolar Invertase Is Required for Cotton Fiber and Arabidopsis Root Elongation through Osmotic Dependent and Independent Pathways, Respectively

“…However, experimental evidence directly supporting this hypothesis is lacking due, in part, to the complexity of multicellular plant tissues . Here, we provide an example that higher activity of VIN activity is likely required for rapid elongation of the singlecelled cotton fibers, taking advantage of its accessibility and extraordinary magnitude of cell expansion (Ruan, 2007). Second, despite the fact that VIN cDNAs have been cloned from a wide range of plant species, to our knowledge there have been no reports thus far that any isolated VIN proteins function in vivo in its native or foreign plants and impact cell growth.…”

“…First, after initiation from the ovule epidermis at anthesis, the single-celled cotton fibers undergo rapid and synchronized unidirectional expansion to several centimeters long by approximately 18 d after anthesis (DAA; Ruan et al, 2001). Hence, a large quantity of homogenous single cells can be readily harvested for studying the control of cell expansion (Ruan, 2007). Second, compelling evidence has indicated a major role of osmotically active solutes in fiber elongation through the generation of cell turgor (Ruan et al, 2004).…”

“…To this end, cotton fiber elongation initiates on the day of anthesis (Ruan, 2007), where it is technically difficult to dissect fiber initials from the seed coat for enzyme assay. Thus, invertase activity was assayed histologically on whole ovule or seed at this early stage.…”

“…Fibers at 5 DAA onward are long enough for freehand harvesting (Ruan, 2007). Thus, enzyme assay was further performed on fibers over their entire elongation period.…”

Unraveling mechanisms of cell expansion linking solute transport, metabolism, plasmodesmtal gating and cell wall dynamics

“…2 Given their unicellular nature, rapid and synchronized growth pattern, high degree of accessibility for harvest and growth measurement, cotton fiber has proven to be an excellent system to study the mechanisms of cell expansion. 3 As an unidirectional cell expansion process, cotton fiber elongation is a result of a complex interplay between cell turgor and cell wall extensibility. 4,5 These two cellular processes require extensive involvement of various transport, metabolic and biosynthetic pathways, and not surprisingly, are coordinately regulated by developmental signals.…”