Endogenous Hypoxia in Lateral Root Primordia Controls Root Architecture by Antagonizing Auxin Signaling in Arabidopsis

As non-photosynthesizing organs, roots are dependent on diffusion of oxygen from the external environment and, in some instances, from the shoot for their aerobic metabolism. Establishment of hypoxic niches in the developing tissues of plants has been postulated as a consequence of insufficient diffusion of oxygen to satisfy the demands throughout development. Here, we report that such niches are established at specific stages of lateral root primordia development in Arabidopsis thaliana grown under aerobic conditions. Using gain- and loss-of-function mutants, we show that ERF-VII transcription factors, which mediate hypoxic responses, control root architecture by acting in cells with a high level of auxin signaling. ERF-VIIs repress the expression of the auxin-induced genes LBD16, LBD18, and PUCHI, which are essential for lateral root development, by binding to their promoters. Our results support a model in which the establishment of hypoxic niches in the developing lateral root primordia contributes to the shutting down of key auxin-induced genes and regulates the production of lateral roots. This study shows that reduced oxygen availability marks lateral root primordia at late developmental stages in Arabidopsis. Exploiting transgenic plants with altered hypoxia responsiveness, it was established that the local activation of ERF-VII transcription factors by low oxygen antagonizes auxin responses and contributes to terminating the primordium development, thus achieving optimal root system architecture.