Root System Architecture from Coupling Cell Shape to Auxin Transport

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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. Plant architecture is determined by where shoots or roots form along the main axis, but the mechanism responsible for lateral root initiation has long puzzled biologists. Here, we show that stretching root cells initiates changes in hormone transport, leading to lateral root initiation in plants, thereby solving a 120-year-old mystery: the mechanism of lateral root initiation. Our data reveal that physical tissue deformation is sufficient to induce chemical changes that unleash biological responses leading to new organ formation. When roots bend, concentrations of the plant hormone auxin increase along the outside of the bend. A complex auxin flux pattern is generated that further enhances auxin levels through localized reflux loops. Auxin importers—AUX1—and efflux carriers—PIN proteins—are known to be regulated by auxin. AUX1 up-regulation enhances the auxin maxima that specify the lateral root founder cells at the bend, while PIN down-regulation modulates the lateral spacing of the roots along the main root axis. This study shows that the biological regulation behind pattern formation can be a result of entangled hierarchies, explaining both the inner/outer spacing, lateral inhibition, and dynamics of lateral root initiation.