The Control of Single-Celled Cotton Fiber Elongation by Developmentally Reversible Gating of Plasmodesmata and Coordinated Expression of Sucrose and K⁺ Transporters and Expansin

Abstract

Each cotton fiber is a single cell that elongates to 2.5 to 3.0 cm from the seed coat epidermis within ‫ف‬ 16 days after anthesis (DAA). To elucidate the mechanisms controlling this rapid elongation, we studied the gating of fiber plasmodesmata and the expression of the cell wall-loosening gene expansin and plasma membrane transporters for sucrose and K ؉ , the major osmotic solutes imported into fibers. Confocal imaging of the membrane-impermeant fluorescent solute carboxyfluorescein (CF) revealed that the fiber plasmodesmata were initially permeable to CF (0 to 9 DAA), but closed at ‫ف‬ 10 DAA and re-opened at 16 DAA. A developmental switch from simple to branched plasmodesmata was also observed in fibers at 10 DAA. Coincident with the transient closure of the plasmodesmata, the sucrose and K ϩ transporter genes were expressed maximally in fibers at 10 DAA with sucrose transporter proteins predominately localized at the fiber base. Consequently, fiber osmotic and turgor potentials were elevated, driving the rapid phase of elongation. The level of expansin mRNA, however, was high at the early phase of elongation (6 to 8 DAA) and decreased rapidly afterwards. The fiber turgor was similar to the underlying seed coat cells at 6 to 10 DAA and after 16 DAA. These results suggest that fiber elongation is initially achieved largely by cell wall loosening and finally terminated by increased wall rigidity and loss of higher turgor. To our knowledge, this study provides an unprecedented demonstration that the gating of plasmodesmata in a given cell is developmentally reversible and is coordinated with the expression of solute transporters and the cell wall-loosening gene. This integration of plasmodesmatal gating and gene expression appears to control fiber cell elongation. INTRODUCTIONA unique feature of cotton seed development is that ‫ف‬ 30% of the ovule epidermal cells initiate into fibers from the outermost layer of integument at anthesis (See Figure 1A). Each cotton fiber is a single cell and elongates from 10 to 15 m up to 2.5 to 3.0 cm by ‫ف‬ 16 days after anthesis (DAA) before it switches to secondary cell wall cellulose synthesis (Basra and Malik, 1984;Tiwari and Wilkins, 1995). The rate of fiber elongation and the final length attained are well above that commonly seen for plant cells (Cosgrove, 1997) and render it perhaps the longest single cell in higher plants. Thus, the cotton fiber represents a unique system in which to study not only carbon partitioning to cellulose synthesis (Delmer and Amor, 1995;Ruan et al., 1997) but also the control of cell elongation without the complication of cell division and multicellular development. Apart from its significance in understanding basic cell biology, elucidating the cellular and molecular basis of fiber elongation could also identify potential targets for genetic manipulation of fiber length, a key determinant of fiber yield and quality.The rapid fiber elongation is believed to be driven by high turgor (Dhindsa et al., 1975;Ruan and Chourey, 1998;Smart et al., 19...

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

“…2,14 Potassium and sucrose are imported from the underlying seed coat cells, either symplasmically through the plasmodesmata (PD) or apoplasmically across cell wall space and plasma membrane by their respective transporters, energized by the plasma membrane and tonoplast H + -ATPases, respectively. 4,5 GhKT1, encodes a cotton K + transporter, is weakly expressed in fibers at 6 DAA when the PD are open. However, its mRNA abundance increases significantly at 10 DAA when the PD are closed and then rapidly decreases to undetectable level at 16 DAA when the PD are re-opened (Fig.…”

“…6 Cytological studies, along with transcriptional investigations, revealed that after a slow start, the elongation rate of cotton fiber increases at ~2-3 DAA followed with a log phase during the first ten days. 1,7 The elongation reaches the maximal rate at ~10-15 DAA 5 and rapidly declines at ~16 DAA onwards when fibers switch to intensive secondary cell wall cellulose biosynthesis. 5,8 The rate and duration of fiber elongation establish the final length attained, which is a key factor determining fiber quality and yield.…”

“…1,7 The elongation reaches the maximal rate at ~10-15 DAA 5 and rapidly declines at ~16 DAA onwards when fibers switch to intensive secondary cell wall cellulose biosynthesis. 5,8 The rate and duration of fiber elongation establish the final length attained, which is a key factor determining fiber quality and yield.…”

“…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. 6 Cytological studies, along with transcriptional investigations, revealed that after a slow start, the elongation rate of cotton fiber increases at ~2-3 DAA followed with a log phase during the first ten days.…”

“…Over the last two decades, great effort has been made to identify genes and cellular mechanisms controlling fiber elongation, primarily focusing on transport of solutes into 5,9 and metabolism within fiber cytoplasm. 10,11 However, little is known how osmotically active solutes are accumulated in the vacuole driving the influx of water for cell expansion.…”