Targeted cell elimination reveals an auxin-guided biphasic mode of lateral root initiation

Abstract

To sustain a lifelong ability to initiate organs, plants retain pools of undifferentiated cells with a preserved proliferation capacity. The root pericycle represents a unique tissue with conditional meristematic activity, and its tight control determines initiation of lateral organs. Here we show that the meristematic activity of the pericycle is constrained by the interaction with the adjacent endodermis. Release of these restraints by elimination of endodermal cells by single-cell ablation triggers the pericycle to re-enter the cell cycle. We found that endodermis removal substitutes for the phytohormone auxin-dependent initiation of the pericycle meristematic activity. However, auxin is indispensable to steer the cell division plane orientation of new organ-defining divisions. We propose a dual, spatiotemporally distinct role for auxin during lateral root initiation. In the endodermis, auxin releases constraints arising from cell-to-cell interactions that compromise the pericycle meristematic activity, whereas, in the pericycle, auxin defines the orientation of the cell division plane to initiate lateral roots.

Lateral Root Priming Synergystically Arises from Root Growth and Auxin Transport Dynamics

“…The priming mechanism described here fits well with earlier experimental observations demonstrating the importance of auxin transport [De Smet et al, 2007,Laskowski et al, 2008,Marhavý et al, 2013, Marhavý et al, 2014, Marhavý et al, 2016 and of auxin signaling in the vasculature [Dubrovsky et al, 2008, Goh et al, 2012 for LR priming, as well as with research demonstrating the impact of IBA production on the amplitude, and to a lesser extent the frequency of priming oscillation [Xuan et al, 2015, Xuan et al, 2016. According to our model, blocking auxin transport will abolish the reflux loop and hence the existence of a proper auxin loading domain, while blocking auxin signaling will abolish events downstream of auxin loading.…”

Periodic Lateral Root Priming: What Makes It Tick?

“…Recent findings suggest that mechanical interactions between the pericycle and overlaying endodermis prevent general, widespread pericycle cell cycle activation and that an elevated auxin response is required to overcome these constraints and enable lateral root initiation (Vermeer et al, 2014;Marhavý et al, 2016). In addition, an elevated auxin response is necessary for reorientation of subsequent divisions to generate correct lateral root primordia development (Marhavý et al, 2016).…”

“…Recent findings suggest that mechanical interactions between the pericycle and overlaying endodermis prevent general, widespread pericycle cell cycle activation and that an elevated auxin response is required to overcome these constraints and enable lateral root initiation (Vermeer et al, 2014;Marhavý et al, 2016). In addition, an elevated auxin response is necessary for reorientation of subsequent divisions to generate correct lateral root primordia development (Marhavý et al, 2016). Because lateral root initiation takes place in a region of the root that has a low level of auxin response (Dubrovsky et al, 2006(Dubrovsky et al, , 2011, it has been suggested that the primary function of lateral root priming is to produce regularly inter spaced patches of cells with an enhanced capacity to respond to auxin, thereby conditioning these cells to respond to auxin levels to which surrounding pericycle cells are insensitive (Van Norman et al, 2013) and enabling them to start the divisions necessary for lateral root initiation.…”

“…Auxin synthesis, transport, and response play key roles in many of these stages, including the transition to lateral root initiation (DeSmet et al, 2010;Ditengou et al, 2008;Dubrovsky et al, 2008;Goh et al, 2012;Laskowski et al, 2008;Lavenus et al, 2013;Marhavý et al, 2013Marhavý et al, , 2014Marhavý et al, , 2016Pérez-Torres et al, 2008). Increases in auxin response activate expression of genes including the lateral root-inducing transcription factor GATA23 (De Rybel et al, 2010) and enable the onset of pericycle cell divisions (Vermeer et al, 2014;Marhavý et al, 2016).…”

“…Increases in auxin response activate expression of genes including the lateral root-inducing transcription factor GATA23 (De Rybel et al, 2010) and enable the onset of pericycle cell divisions (Vermeer et al, 2014;Marhavý et al, 2016). In later stages of lateral root development, cell wall loosening is attributed to auxin export (C) In protoxylem cells of the basal meristem, cells undergo temporal priming oscillations in auxin concentration and/or auxin response levels as well as oscillations in the expression of many other genes that lead these cells to pass on a priming signal to the overlying pericycle cells.…”