Auxin Influx Carriers Control Vascular Patterning and Xylem Differentiation in Arabidopsis thaliana

Abstract

Auxin is an essential hormone for plant growth and development. Auxin influx carriers AUX1/LAX transport auxin into the cell, while auxin efflux carriers PIN pump it out of the cell. It is well established that efflux carriers play an important role in the shoot vascular patterning, yet the contribution of influx carriers to the shoot vasculature remains unknown. Here, we combined theoretical and experimental approaches to decipher the role of auxin influx carriers in the patterning and differentiation of vascular tissues in the Arabidopsis inflorescence stem. Our theoretical analysis predicts that influx carriers facilitate periodic patterning and modulate the periodicity of auxin maxima. In agreement, we observed fewer and more spaced vascular bundles in quadruple mutants plants of the auxin influx carriers aux1lax1lax2lax3. Furthermore, we show AUX1/LAX carriers promote xylem differentiation in both the shoot and the root tissues. Influx carriers increase cytoplasmic auxin signaling, and thereby differentiation. In addition to this cytoplasmic role of auxin, our computational simulations propose a role for extracellular auxin as an inhibitor of xylem differentiation. Altogether, our study shows that auxin influx carriers AUX1/LAX regulate vascular patterning and differentiation in plants.

Author Summary

The vascular tissues in the shoot of Arabidopsis thaliana (Arabidopsis) plants are organized in vascular bundles, disposed in a conserved periodic radial pattern. It is known that this pattern emerges due to the accumulation of the phytohormone auxin, which is actively transported by the so-called efflux and the influx carriers. Efflux carriers facilitate polar transport of auxin from inside the cell to the extracellular space, while influx carriers pump auxin from outside the cell to its interior in a non-polar manner. Although a role for auxin efflux carriers in the emergence of this pattern has been recognized, the role of auxin influx carriers has remained hitherto neglected. In this study, we combine theoretical and experimental approaches to unravel the role of the auxin influx carriers in the formation of plant vasculature. Our analysis uncovers primary roles for the auxin influx carriers in vascular patterning, revealing that auxin influx carriers modulate both patterning and the differentiation of the water transporting vascular cells, known as xylem cells.