Integration of transport-based models for phyllotaxis and midvein formation

Abstract

The plant hormone auxin mediates developmental patterning by a mechanism that is based on active transport. In the shoot apical meristem, auxin gradients are thought to be set up through a feedback loop between auxin and the activity and polar localization of its transporter, the PIN1 protein. Two distinct molecular mechanisms for the subcellular polarization of PIN1 have been proposed. For leaf positioning (phyllotaxis), an ''up-the-gradient'' PIN1 polarization mechanism has been proposed, whereas the formation of vascular strands is thought to proceed by ''with-the-flux'' PIN1 polarization. These patterning mechanisms intersect during the initiation of the midvein, which raises the question of how two different PIN1 polarization mechanisms may work together. Our detailed analysis of PIN1 polarization during midvein initiation suggests that both mechanisms for PIN1 polarization operate simultaneously. Computer simulations of the resulting dual polarization model are able to reproduce the dynamics of observed PIN1 localization. In addition, the appearance of high auxin concentration in our simulations throughout the initiation of the midvein is consistent with experimental observation and offers an explanation for a long-standing criticism of the canalization hypothesis; namely, how both high flux and high concentration can occur simultaneously in emerging veins.[Keywords: Auxin; transport; PIN1; phyllotaxis; vein; computer simulation] Supplemental material is available at http://www.genesdev.org.

Brassinosteroid signaling and auxin transport are required to establish the periodic pattern of Arabidopsis shoot vascular bundles

“…Based on these studies, our model takes into account auxin polar transport between cells and the apoplast and passive diffusion across the apoplast (Materials and Methods). An analysis of the model shows that appropriate asymmetric localization of efflux carriers is able to elicit auxin maxima ( Recently, support for this kind of localization has been reported in both tomato and Arabidopsis where lateral polarization of efflux carrier protein PIN1 toward the developing vasculature has been observed (35). Taken together, these data propose efflux carrier localization as promoters of auxin maxima in shoot vascular bundles.…”

Auxin depletion from leaf primordia contributes to organ patterning

“…PIN1 mediated auxin transport in the SAM from all directions toward an incipient primordium acts to trigger the formation of a new primordium (17,36). However, PIN1 polarity reverses and directs back toward the meristem center from early developing leaves, although the exact stage at which this reversal occurs is not known (17,22,23,37).…”

Context, Specificity, and Self-Organization in Auxin Response

“…This demands an opposite "with-the-flux" polarization of PIN proteins which is part of a more general concept of self-organization in auxin biology known as the canalization hypothesis which proposes that increasingly narrow paths or "canals" for auxin transport can be formed by the action of positive feedback loops acting at the level of individual cells (Sachs 2000;Sauer et al 2006). Recent modeling work evaluating these seemingly incompatible arrangements of PINs has raised the possibility that both mechanisms could operate simultaneously in a given cell with the balance of activity between them determined by thresholds of auxin concentration (Bayer et al 2009). Importantly, a significant proportion of the basipetal auxin flow is refluxed back into the central acropetal flow at the transition zone (TZ).…”

“…In this way a convergence point is formed that marks precisely the incipient primordium and once a threshold concentration of auxin is reached, primordium initiation is begun (Reinhardt et al 2003;Bayer et al 2009). In addition to this, experimental and mathematical modeling approaches have identified the possibility of a second auxin-dependent developmental transition in the primordium program, triggered once an even higher auxin concentration threshold is reached at the convergence point (Bayer et al 2009): Midway through primordium development auxin flow switches from predominantly toward the convergence point in the L1 layer to away from it and down into the underlying tissues as part of the specification of the vasculature that will form the midvein of the developing leaf (Sachs 2000;Reinhardt et al 2003) (Fig. 4A).…”