A tightly regulated auxin signaling landscape is required for spatial accommodation of lateral roots in Arabidopsis

Abstract

In Arabidopsis thaliana, lateral root (LR) development requires spatial accommodation responses in overlying endodermal cells. This includes loss of cell volume whilst maintaining membrane integrity to allow the expansion of the underlying LR primordia (LRPs). These accommodation responses are regulated by auxin-mediated signaling, specifically through Aux/IAA proteins, involving IAA3/SHY2. Plants that express a stabilized version of SHY2 (shy2-2) in differentiated endodermal cells, CASP1pro::shy2-2 plants, fail to make LRs. Exogenous treatment with 1-naphthaleneacetic acid (NAA) was reported to partially restore LR formation in this spatial accommodation mutant. Using treatments with auxins having different transport properties, such as NAA, indole-3-acetic acid (IAA), and 2,4-dichlorophenoxyacetic acid (2,4-D), we assessed the ability of each auxin to rescue LR formation in CASP1pro::shy2-2 roots. This revealed that IAA is the most effective in partially restoring LR development, NAA is effective in inducing LRPs but cannot maintain their canonical phenotype, whereas 2,4-D induces non-controlled cell divisions. In addition, we show that in CASP1pro::shy2-2 roots, AUX1 appears to be repressed in the zone where oscillation of the auxin response has been described. Our study advances the understanding of auxin-regulated spatial accommodation mechanisms during LRP formation and highlights the complex interplay of auxin transport and signaling in bypassing the endodermal constraints.