A reflux-and-growth mechanism explains oscillatory patterning of lateral root branching sites

• Published in: Developmental cell Vol. 56; no. 15; pp. 2176 - 2191.e10
• Main Authors: van den Berg, Thea, Yalamanchili, Kavya, de Gernier, Hugues, Santos Teixeira, Joana, Beeckman, Tom, Scheres, Ben, Willemsen, Viola, ten Tusscher, Kirsten
• Format: Journal Article
• Language: English
• Published: Elsevier Inc 09.08.2021
• Subjects: auxin transport; computational modeling; experimental validation; lateral root priming; oscillatory priming dynamics; periodic developmental patterning; plant root branching; root growth dynamics; oscillatory priming dynamics; experimental validation; lateral root priming; plant root branching; periodic developmental patterning; computational modeling; auxin transport; root growth dynamics
• ISSN: 1534-5807; 1878-1551
• DOI: 10.1016/j.devcel.2021.07.005

Modular, repetitive structures are a key component of complex multicellular body plans across the tree of life. Typically, these structures are prepatterned by temporal oscillations in gene expression or signaling. Although a clock-and-wavefront mechanism was identified and plant leaf phyllotaxis arises from a Turing-type patterning for vertebrate somitogenesis and arthropod segmentation, the mechanism underlying lateral root patterning has remained elusive. To resolve this enigma, we combined computational modeling with in planta experiments. Intriguingly, auxin oscillations automatically emerge in our model from the interplay between a reflux-loop-generated auxin loading zone and stem-cell-driven growth dynamics generating periodic cell-size variations. In contrast to the clock-and-wavefront mechanism and Turing patterning, the uncovered mechanism predicts both frequency and spacing of lateral-root-forming sites to positively correlate with root meristem growth. We validate this prediction experimentally. Combined, our model and experimental results support that a reflux-and-growth patterning mechanism underlies lateral root priming. [Display omitted] •Lateral root priming arises from the interplay of root growth and auxin transport•Auxin loading preferentially occurs in narrow elongated cells of the vasculature•Root growth produces periodic variations in cell length and, hence, auxin loading•Experiments support this model and not a Turing pattern or clock-and-wavefront model Combining computational modeling with experiments, van den Berg et al. deciphered the mechanism underlying periodic plant root system branching. The authors demonstrated that the interplay between auxin transport and root tip growth dynamics gives rise to periodic elevations in the hormone auxin, prepatterning future lateral-root-forming sites.