Cell proliferation and hair tip growth in the Arabidopsis root are under mechanistically different forms of redox control

Abstract

We provide evidence that the tripeptide thiol glutathione (GSH) participates in the regulation of cell division in the apical meristem of Arabidopsis roots. Exogenous application of micromolar concentrations of GSH raised the number of meristematic cells undergoing mitosis, while depletion of GSH had the opposite effect. A role for endogenous GSH in the control of cell proliferation is also provided by mapping of GSH levels in the root meristem using the GSH-specific dye monochlorobimane and confocal laser scanning microscopy. High levels of GSH were associated with the epidermal and cortical initials and markedly lower levels in the quiescent center. The mechanisms controlling cell division could also be triggered by other reducing agents: ascorbic acid and dithiothreitol. Our data also reveal significant plasticity in the relationship between the trichoblast cell length and the hair it subtends in response to alterations in intracellular redox homeostasis. While mechanisms that control trichoblast elongation are inf luenced by nonspecific redox couples, root hair tip growth has a more specific requirement for sulfhydryl groups. The responses we describe here may represent the extremes of redox control of root plasticity and would allow the root to maintain exploration of the soil under adverse conditions with minimal cell divisions and root hair production or capitalize on a favorable environment by production of numerous long hairs. Redox sensing of the environment and subsequent redox-dependent modulation of growth and development may be crucial components in the strategies plants have evolved for survival in a f luctuating environment.

Defects in a New Class of Sulfate/Anion Transporter Link Sulfur Acclimation Responses to Intracellular Glutathione Levels and Cell Cycle Control

“…Based on these findings, we speculate that aberrant glutathione levels and redox homeostasis cause the increased division and small-cell phenotypes observed in the smt15-1 mutant. Supporting this hypothesis are numerous reports on the close association between cell proliferation and elevated glutathione levels and high GSH-GSSG ratios (Mauro et al, 1969;Kosower and Kosower, 1978;Suthanthiran et al, 1990;Sánchez-Fernández et al, 1997;May et al, 1998;Nkabyo et al, 2002). We have not been able to examine temporal redox control at a finer scale in wild-type and smt15-1 cells, as has been done in budding yeast, where redox and respiratory activity cycle with a period of about 40 min (Tu et al, 2005).…”

Infection and Invasion of Roots by Symbiotic, Nitrogen-Fixing Rhizobia during Nodulation of Temperate Legumes

“…Thus, the RHD2 NADPH oxidase may be responsible for generating ROS that in turn help establish tip-associated calcium gradients by activating Ca 2ϩ channels needed for root hair elongation. This gives a mechanistic explanation for earlier observations that root hair length and root hair density along the root is influenced by redox conditions (28,139).…”

Reactive oxygen species and ethylene play a positive role in lateral root base nodulation of a semiaquatic legume

“…Accordingly, axillary root hair growth on hydroponic roots of S. rostrata was induced by exogenous ethylene and H 2 O 2 . Also in Arabidopsis thaliana, ethylene plays a role in root hair growth (33), and changes in the redox status of the environment may influence induction of root hair elongation (34).…”