Flux-Based Transport Enhancement as a Plausible Unifying Mechanism for Auxin Transport in Meristem Development

Abstract

Plants continuously generate new organs through the activity of populations of stem cells called meristems. The shoot apical meristem initiates leaves, flowers, and lateral meristems in highly ordered, spiralled, or whorled patterns via a process called phyllotaxis. It is commonly accepted that the active transport of the plant hormone auxin plays a major role in this process. Current hypotheses propose that cellular hormone transporters of the PIN family would create local auxin maxima at precise positions, which in turn would lead to organ initiation. To explain how auxin transporters could create hormone fluxes to distinct regions within the plant, different concepts have been proposed. A major hypothesis, canalization, proposes that the auxin transporters act by amplifying and stabilizing existing fluxes, which could be initiated, for example, by local diffusion. This convincingly explains the organised auxin fluxes during vein formation, but for the shoot apical meristem a second hypothesis was proposed, where the hormone would be systematically transported towards the areas with the highest concentrations. This implies the coexistence of two radically different mechanisms for PIN allocation in the membrane, one based on flux sensing and the other on local concentration sensing. Because these patterning processes require the interaction of hundreds of cells, it is impossible to estimate on a purely intuitive basis if a particular scenario is plausible or not. Therefore, computational modelling provides a powerful means to test this type of complex hypothesis. Here, using a dedicated computer simulation tool, we show that a flux-based polarization hypothesis is able to explain auxin transport at the shoot meristem as well, thus providing a unifying concept for the control of auxin distribution in the plant. Further experiments are now required to distinguish between flux-based polarization and other hypotheses.

Regulated transport as a mechanism for pattern generation: Capabilities for phyllotaxis and beyond

“…is still an open question, but recent work has investigated the possibility of a unified description [Merks et al, 2007, Stoma et al, 2008.…”

Multiscale modelling of auxin transport in the plant-root elongation zone

“…Many computational cell-scale models are being developed to investigate auxin transport (de Reuille et al 2006;Feugier and Iwasa 2006;Feugier et al 2005;Grieneisen et al 2007;Heisler and Jönsson 2006;Jönsson et al 2006;Kramer 2004Kramer , 2009Laskowski et al 2008;Merks et al 2007;Mironova et al 2010;Perrine-Walker et al 2010;Rolland-Lagan and Prusinkiewicz 2005;Smith et al 2006;Stoma et al 2008;Swarup et al 2005); however, little has been done to determine the corresponding tissue-scale descriptions. In this paper, we demonstrate the potential of using (analytical) multiscale methods to simplify an auxin-transport model and to identify the combinations of cell-scale processes that govern the tissue-scale auxin flux.…”

“…The labels C, F, K, and M are provided to clarify the discussion in Sect. 2 Swarup et al 2005), vein formation (Feugier et al 2005;Feugier and Iwasa 2006;Merks et al 2007;Mitchison 1980a;Mitchison et al 1981;Rolland-Lagan and Prusinkiewicz 2005) and organ initiation (de Reuille et al 2006;Heisler and Jönsson 2006;Jönsson et al 2006;Laskowski et al 2008;Stoma et al 2008;Newell et al 2008;Perrine-Walker et al 2010;Smith et al 2006;Stoma et al 2008), for example. Early studies (Goldsmith et al 1981;Martin et al 1990;Mitchison 1980b) considered only a single line of cells, with auxin diffusion within the cytoplasms and with passive and carrier-mediated transport across the cell membranes; these showed how the efflux carriers increase the tissue-scale auxin flux.…”

“…Early studies (Goldsmith et al 1981;Martin et al 1990;Mitchison 1980b) considered only a single line of cells, with auxin diffusion within the cytoplasms and with passive and carrier-mediated transport across the cell membranes; these showed how the efflux carriers increase the tissue-scale auxin flux. More recent studies have considered more complex tissue geometries and have incorporated apoplastic diffusion Jönsson et al 2006;Kramer 2004;Laskowski et al 2008;Swarup et al 2005), saturable carrier-mediated transport (de Reuille et al 2006;Feugier et al 2005;Jönsson et al 2006;Merks et al 2007;Smith et al 2006), cytoplasmic structure (Kramer 2004;Perrine-Walker et al 2010), cell growth (Chavarrıa-Krauser et al 2005;Grieneisen et al 2007;Jönsson et al 2006;Mironova et al 2010;Stoma et al 2008), auxin production and degradation (Feugier and Iwasa 2006;Feugier et al 2005;Perrine-Walker et al 2010;Heisler and Jönsson 2006;Jönsson et al 2006;Smith et al 2006;Stoma et al 2008) and dynamics of the efflux carriers Jönsson et al 2006;Kramer 2009;Merks et al 2007;Mironova et al 2010;Stoma et al 2008).…”

Effects of explant, media and growth regulators on in vitro regeneration and antioxidant activity of Juniperus phoenicea

“…The expression pattern of auxin conjugate synthetases and hydrolases was reported in many plants and suggested their overlapping roles in the development of plant organs (Ludwig-Müller, 2011). It is also possible that exogenously applied cytokinins did not induce the expression of tissue-specific auxin carriers necessary for an auxin maximum for the tissue threshold of rooting competence as a specific auxin pattern (Stoma et al, 2008) in comparison to the effects induced by TIBA and DM. The promoting effects of TIBA and DM on shoot and root formation, in addition to callus induction, could be beneficial for the study of the developmental biology of plant organs in relation to the action of hormones in general and of auxins in particular.…”