Oscillating Gene Expression Determines Competence for Periodic Arabidopsis Root Branching

Abstract

Plants and animals produce modular developmental units in a periodic fashion. In plants, lateral roots form as repeating units along the root primary axis; however, the developmental mechanism regulating this process is unknown. We found that cyclic expression pulses of a reporter gene mark the position of future lateral roots by establishing prebranch sites and that prebranch site production and root bending are periodic. Microarray and promoter-luciferase studies revealed two sets of genes oscillating in opposite phases at the root tip. Genetic studies show that some oscillating transcriptional regulators are required for periodicity in one or both developmental processes. This molecular mechanism has characteristics that resemble molecular clock-driven activities in animal species.Formation of periodic modular structures is a common developmental feature in both animals and plants (1,2). The body axis of many metazoans-including species of arthropods, annelids, and vertebrates-is organized into segments. This organization is established during embryogenesis by successive addition of segments to an elongating posterior body region (3). In plants, branching of shoots and roots during postembryonic development produces repeating units (phytomers and lateral roots, respectively) along the growing longitudinal axis. Leaves are generated in a regular phyllotactic pattern, and lateral roots (LRs) are continuously produced from the primary root (Fig. 1A) as it grows, following the gravity vector (4).In vertebrates, segmentation is coordinated by a molecular clock that converts temporal information into a periodic spatial pattern, which precisely positions somites along the anterior-posterior axis (3,5). In the plant shoot apical meristem, there is evidence that

Three-Dimensional Root Phenotyping with a Novel Imaging and Software Platform

“…Root circumnutation describes the tendency of roots to grow downward through their growth medium along a helical axis and has been mainly studied by analyzing the skewing and periodic waving patterns of the primary roots of Arabidopsis (Arabidopsis thaliana) plants grown on 2D agar plate systems. While the causes of the observed skewing and waving patterns remain under debate, at present they have mainly been attributed to three intrinsic growth responses, circumnutation, gravitropism, and negative thigmotropism (Migliaccio and Piconese, 2001;Oliva and Dunand, 2007), and are suggested to be linked with the recent discovery of oscillating gene expression cycles that also impact the periodic establishment of lateral root prebranching sites along the primary root of Arabidopsis (Moreno-Risueno et al, 2010).…”

Ontogeny of the Maize Shoot Apical Meristem

“…There is little variation in the total number of genes represented among the six stages; the transition stage comprised the largest number of individual gene transcripts (16,454), whereas the coleoptile stage had the fewest (15,952). Oscillations in gene expression, wherein certain genes are used reiteratively during development, have been demonstrated to impose some limitations on the use of transcriptomic analyses of developmental ontogeny (Brady et al, 2007;Moreno-Risueno et al, 2010). Indeed, six-way comparisons of the transcriptional data sets identified 12,135 genes that are common to all samples ( Figure 2A).…”

cis-Cinnamic Acid Is a Novel, Natural Auxin Efflux Inhibitor That Promotes Lateral Root Formation

“…Arabidopsis ecotype Columbia (Col-0) was used, unless stated elsewhere. Following transgenic lines were in the same ecotype: DII-VENUS, pDR5rev:GFP, pDR5:LUC, pGATA23:GUS, pGAZAT:GUS, pKNOLLE:KNOLLE-GFP, p35S:iaaL, slr, arf7 arf19, and tir1 afb2 afb3 (Romano et al, 1991;Lukowitz et al, 1996;Fukaki et al, 2002;Friml et al, 2003;Dharmasiri et al, 2005;González-Carranza et al, 2007;Okushima et al, 2007;De Rybel et al, 2010;Moreno-Risueno et al, 2010;Brunoud et al, 2012). The transgenic line pCYCB1:GUS was in the ecotype Landsberg erecta (Ler; Colón-Carmona et al, 1999).…”