Auxin-dependent control of a plasmodesmal regulator creates a negative feedback loop modulating lateral root emergence

Abstract

Lateral roots originate from initial cells deep within the main root and must emerge through several overlying layers. Lateral root emergence requires the outgrowth of the new primordium (LRP) to coincide with the timely separation of overlying root cells, a developmental program coordinated by the hormone auxin. Here, we report that in Arabidopsis thaliana roots, auxin controls the spatiotemporal expression of the plasmodesmal regulator PDLP5 in cells overlying LRP, creating a negative feedback loop. PDLP5, which functions to restrict the cellto-cell movement of signals via plasmodesmata, is induced by auxin in cells overlying LRP in a progressive manner. PDLP5 localizes to plasmodesmata in these cells and negatively impacts organ emergence as well as overall root branching. We present a model, incorporating the spatiotemporal expression of PDLP5 in LRP-overlying cells into known auxin-regulated LRP-overlying cell separation pathways, and speculate how PDLP5 may function to negatively regulate the lateral root emergence process.

Uncharted routes: exploring the relevance of auxin movement via plasmodesmata

“…Higher auxin levels might therefore be present in those cells in the mutant. Considering the positive role of auxin in altering cell wall components to facilitate passage of the new root across the tissues of the primary one (reviewed in Péret et al, 2009), this well agrees with the observed increased lateral root emergence in the mutant (Sager et al, 2020).…”

“…It was shown that ectopic induction of PDCB1 resulted in reduced emergence, likely because of callose induction in tissues overlying LRPs (Maule et al, 2013). This was confirmed in Sager et al (2020) by overexpressing another protein, PD localised protein (PDLP) 5. When the native domain of expression of PDLP5 was studied, the authors observed that signal occurred in cell layers above LRPs and accompanied lateral root emergence.…”

“…These processes are achieved via combinations of auxin maxima, gradients and overall signalling (reviewed in Lavenus et al, 2013). Symplastic connectivity of the lateral root primordium (LRP) and surrounding tissues also plays key roles in lateral root development (Benitez-Alfonso et al, 2013;Sager et al, 2020). Specifically, LRPs become fully isolated via callose accumulation around stages IV-V (Benitez-Alfonso et al, 2013).…”

Do Plasmodesmata Play a Prominent Role in Regulation of Auxin-Dependent Genes at Early Stages of Embryogenesis?

“…Callose-dependent changes of the PD aperture are responsible for the directional diffusion of auxin in midrib and petiole epidermis cells [ 49 ], and higher PD permeability for auxin was seen in gsl8 mutants, compared to wild-type plants [ 50 ]. Callose synthesis was also found to be indispensable during the formation of the apical-basal axis and the development of the embryonic root [ 45 , 46 , 51 , 52 ].…”

Metabolic Cellular Communications: Feedback Mechanisms between Membrane Lipid Homeostasis and Plant Development

“…Lipid characterization of isolated plasmodesmata revealed that they are significantly enriched in sterols and sphingolipids containing α-hydroxylated VLCFAs and phytosphinganine (tri-hydroxylated long chain base t18:0) (Grison et al, 2015;Liu et al, 2020). Phytosphinganine binds plasmodesmata-located protein 5 (PDLP5) which regulates plasmodesmata cell-to-cell connectivity (Liu et al, 2020;Sager et al, 2020). Furthermore, the sphingolipid biosynthesis phloem unloading modulator (plm) mutant has reduced level of VLCFA-ceramides and displays enhanced cell-to-cell trafficking between the pericycle and the endodermis (Yan et al, 2019).…”