Root System Architecture from Coupling Cell Shape to Auxin Transport

Abstract

Lateral organ position along roots and shoots largely determines plant architecture, and depends on auxin distribution patterns. Determination of the underlying patterning mechanisms has hitherto been complicated because they operate during growth and division. Here, we show by experiments and computational modeling that curvature of the Arabidopsis root influences cell sizes, which, together with tissue properties that determine auxin transport, induces higher auxin levels in the pericycle cells on the outside of the curve. The abundance and position of the auxin transporters restricts this response to the zone competent for lateral root formation. The auxin import facilitator, AUX1, is up-regulated by auxin, resulting in additional local auxin import, thus creating a new auxin maximum that triggers organ formation. Longitudinal spacing of lateral roots is modulated by PIN proteins that promote auxin efflux, and pin2,3,7 triple mutants show impaired lateral inhibition. Thus, lateral root patterning combines a trigger, such as cell size difference due to bending, with a self-organizing system that mediates alterations in auxin transport.

The Ectomycorrhizal FungusLaccaria bicolorStimulates Lateral Root Formation in Poplar and Arabidopsis through Auxin Transport and Signaling

“…Second, LRI itself, comprising cell cycle reactivation of the founder cells and subsequent further cell divisions, occurs in more proximal regions of the root and leads to the formation of a LR primordium (Malamy and Benfey, 1997). Finally, the new LR emerges after having grown through the cortex and epidermis of the parental root.The phytohormone auxin (indole-3-acetic acid [IAA]) is considered to be one of the main triggers regulating all of the different steps of LR formation (Bainbridge et al, 2008;Ditengou et al, 2008;Laskowski et al, 2008;Nibau et al, 2008). For instance, the acquisition of founder cell identity, cell cycle reactivation, and LR emergence all correlate with and require local auxin accumulation in specific cell types (Dubrovsky et al, 2008;Fukaki and Tasaka, 2009).…”

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 majority of previous models use the same value for the permeability due to the influx carriers, and therefore we set P AU X 1 = 0.2 cm h −1 = 0.56 µm s −1 Kramer 2004;Swarup et al 2005). In contrast, various values are used for the permeability due to the efflux carriers, including 0.124 µm s −1 (Goldsmith et al 1981;Jönsson et al 2006), 0.27 µm s −1 ), 1.4 µm s −1 (Kramer 2004) and 20 µm s −1 (Laskowski et al 2008). Swarup et al (2005) assume that all the epidermal cells (and similarly all the cortical cells and all the endodermal cells) have an efflux-carrier number proportional to the area of the cell membrane, which, as the efflux carriers are present only on the shootward face of the membrane, results in the efflux-carrier density on this face increasing with cell length.…”

“…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).…”