Auxin fluxes through plasmodesmata modify root-tip auxin distribution

Abstract

Auxin is a key signal regulating plant growth and development. It is well established that auxin dynamics depend on the spatial distribution of efflux and influx carriers on the cell membranes. In this study, we employ a systems approach to characterise an alternative symplastic pathway for auxin mobilisation via plasmodesmata, which function as intercellular pores linking the cytoplasm of adjacent cells. To investigate the role of plasmodesmata in auxin patterning, we developed a multicellular model of the Arabidopsis root tip. We tested the model predictions using the DII-VENUS auxin response reporter, comparing the predicted and observed DII-VENUS distributions using genetic and chemical perturbations designed to affect both carrier-mediated and plasmodesmatal auxin fluxes. The model revealed that carriermediated transport alone cannot explain the experimentally determined auxin distribution in the root tip. In contrast, a composite model that incorporates both carrier-mediated and plasmodesmatal auxin fluxes re-capitulates the root-tip auxin distribution. We found that auxin fluxes through plasmodesmata enable auxin reflux and increase total root-tip auxin. We conclude that auxin fluxes through plasmodesmata modify the auxin distribution created by efflux and influx carriers.

ABCB-mediated auxin transport in outer root tissues regulates lateral root spacing inArabidopsis

“…Recently, passive auxin diffusion via plasmodesmata, intercellular pores that linking the cytoplasm of adjacent cells, was shown to markedly improve the accuracy of simulated auxin distribution patterns in the root apical meristem 35 . Therefore, it will be of interest to evaluate the contribution of symplastic connectivity between the radial layers of the root to prebranch site formation and LR spacing.…”

Uncharted routes: exploring the relevance of auxin movement via plasmodesmata

“…1B). In the context of auxin, this was recently highlighted in Mellor et al (2020). The authors, focusing on the root tip of Arabidopsis, compared the observed signal intensity of a DII-VENUS reporter (where fluorescence negatively correlates with auxin concentration) (Brunoud et al, 2012) with that predicted by a modified computational model of them (Band et al, 2014).…”

“…Symplastic auxin movement indeed reduced the sharpness of concentration differences and provided better agreement with those observed experimentally. Specifically, this form of movement was essential to facilitate reflux from the high auxin areas in the outer tissues, where active transporters direct flow shoot-ward, to the inner central tissues where flow is root-ward and the auxin concentration is lower (Mellor et al, 2020). This reflux component was theorised in Grieneisen et al, 2007 and is necessary to retain high auxin concentrations in the root tip, something necessary for many biological processes.…”

“…The transporters also provide an extremely refined and tuneable directionality system at the cellular scale (Zhang et al, 2020; Huang et al, 2010, as examples). PD transport could instead integrate into this picture and explain situations where transporters alone do not seem sufficient to explain the biology of the system (Mellor et al, 2020;Verna et al, 2019;Guenot et al, 2012, as potential examples).…”

Gravity Signaling in Flowering Plant Roots

“…Interestingly, PIN2 also localizes on the tip-facing and inner sides at the DEZ, contributing to an auxin reflux from the shootward stream back into the tip-directed stream [ 54 ]. An alternative cell-to-cell transport via plasmodesmata also enables auxin reflux to the root tip and its accumulation in cells of the quiescent-center and upper columella layers [ 55 ].…”