Periodic root branching in Arabidopsis requires synthesis of an uncharacterized carotenoid derivative

Abstract

In plants, continuous formation of lateral roots (LRs) facilitates efficient exploration of the soil environment. Roots can maximize developmental capacity in variable environmental conditions through establishment of sites competent to form LRs. This LR prepattern is established by a periodic oscillation in gene expression near the root tip. The spatial distribution of competent (prebranch) sites results from the interplay between this periodic process and primary root growth; yet, much about this oscillatory process and the formation of prebranch sites remains unknown. We find that disruption of carotenoid biosynthesis results in seedlings with very few LRs. Carotenoids are further required for the output of the LR clock because inhibition of carotenoid synthesis also results in fewer sites competent to form LRs. Genetic analyses and a carotenoid cleavage inhibitor indicate that an apocarotenoid, distinct from abscisic acid or strigolactone, is specifically required for LR formation. Expression of a key carotenoid biosynthesis gene occurs in a spatially specific pattern along the root's axis, suggesting spatial regulation of carotenoid synthesis. These results indicate that developmental prepatterning of LRs requires an uncharacterized carotenoid-derived molecule. We propose that this molecule functions non-cell-autonomously in establishment of the LR prepattern.root development | patterning | secondary metabolite synthesis A nchorage and uptake of water and soluble nutrients are essential functions of plant root systems and key to plant productivity and survival. The capacity of a root system to carry out these functions can be maximized by iterative root branching. Root branches are formed de novo during primary root growth, which allows for the elaboration of a complex root system that effectively enables the plant to navigate and exploit the resources of diverse, locally variable subterranean environments. Understanding the developmental mechanisms underlying the pattern of root branches has broad significance in both basic and applied research.As with other dicotyledonous plants, formation of a complex root system in the model plant Arabidopsis thaliana (Arabidopsis) occurs through iterative production of branches, or lateral roots (LRs), from the primary root. The simplified root system of Arabidopsis has yielded considerable insight into the cellular events and molecular regulators required for LR formation (recently reviewed in refs.

Regulation of Hormonal Control, Cell Reprogramming, and Patterning during De Novo Root Organogenesis

“…We quantified lateral root capacity. In this assay, the root tip is cut to induce growth of lateral roots as described previously (van Norman et al, 2014). We confirmed, under the microscope, there were no unemerged primordia.…”

Plant adaptations to severely phosphorus-impoverished soils

“…However, the position of the lateral roots is different, and hence, the pattern of signalling compounds inducing lateral-root formation differs. Interestingly, a recent paper reports on a so-far uncharacterised carotenoid derivative required for the periodic branching of Arabidopsis roots [47]. We therefore speculate that either the different periodic production of this carotenoid derivative or a different perception of this molecule comprise at least one of the components required for the production of cluster roots.…”

An Uncharacterized Apocarotenoid-Derived Signal Generated in ζ-Carotene Desaturase Mutants Regulates Leaf Development and the Expression of Chloroplast and Nuclear Genes inArabidopsis

“…Many apocarotenoids produced through these remodeling processes have signaling activities, as they can move to different subcellular compartments in which they perform various biological functions, including modulating developmental processes such as lateral root pattering (Bouvier et al, 2005;Walter et al, 2010;Van Norman et al, 2014). We reasoned that it was possible that an apocarotenoid derived from the linear carotenoids that accumulate in clb5 could generate a signal responsible for the described clb5 phenotypes.…”

“…Whether the CCD4 colocalization or cell-specific expression patterns are important for the generation of this signal is a matter for future research. In addition, recent data showed that the rate-limiting enzymes of the carotenoid pathway, such as PSY, display a particular expression pattern (Van Norman et al, 2014).…”

“…It is known that carotenoids are substrates of enzymatic cleavage, producing different apocarotenoids with diverse signaling functions, such as hormones and volatiles that influence plant development (Walter et al, 2010;Van Norman et al, 2014). Many apocarotenoids are produced by the action of the family of CCD enzymes that catabolize particular carotenoid substrates (Auldridge et al, 2006b;Ramel et al, 2012).…”