The establishment of asymmetry in Arabidopsis lateral root founder cells is regulated by LBD16/ASL18 and related LBD/ASL proteins

Abstract

In most dicot plants, lateral root (LR) formation, which is important for the construction of the plant root system, is initiated from coordinated asymmetric cell divisions (ACD) of the primed LR founder cells in the xylem pole pericycle (XPP) of the existing roots. In Arabidopsis thaliana, two AUXIN RESPONSE FACTORs (ARFs), ARF7 and ARF19, positively regulate LR formation through activation of the plant-specific transcriptional regulators LATERAL ORGAN BOUNDARIES-DOMAIN 16/ASYMMETRIC LEAVES2-LIKE 18 (LBD16/ASL18) and the other related LBD/ASL genes. The exact biological role of these LBD/ASLs in LR formation is still unknown. Here, we demonstrate that LBD16/ASL18 is specifically expressed in the LR founder cells adjacent to the XPP before the first ACD and that it functions redundantly with the other auxin-inducible LBD/ASLs in LR initiation. The spatiotemporal expression of LBD16/ASL18 during LR initiation is dependent on the SOLITARY-ROOT (SLR)/IAA14-ARF7-ARF19 auxin signaling module. In addition, XPP-specific expression of LBD16/ASL18 in arf7 arf19 induced cell divisions at XPP, thereby restoring the LR phenotype. We also demonstrate that expression of LBD16-SRDX, a dominant repressor of LBD16/ASL18 and its related LBD/ASLs, does not interfere in the specification of LR founder cells with local activation of the auxin response, but it blocks the polar nuclear migration in LR founder cells before ACD, thereby blocking the subsequent LR initiation. Taken together, these results indicate that the localized activity of LBD16/ASL18 and its related LBD/ASLs is involved in the symmetry breaking of LR founder cells for LR initiation, a key step for constructing the plant root system.

Plant regeneration: cellular origins and molecular mechanisms

“…5B). The LBDs and WOX5 are also involved in lateral root development, in which locally accumulated auxin promotes the formation of new root meristems from pericycle cells (Goh et al, 2012;Ditengou et al, 2008). These two pathways thus share some key regulators to facilitate the auxin-mediated establishment of root meristems.…”

To branch or not to branch: the role of pre-patterning in lateral root formation

“…An alternative, and not mutually exclusive, hypothesis is that genes oscillating in the pericycle itself have important roles in establishing the LR prepattern. For example, LBD16 is observed to oscillate and was recently reported to have XPP-specific expression and a key role in LR initiation (Goh et al, 2012;Moreno-Risueno et al, 2010). Because the root tissue examined for oscillating transcriptional profiles was specific to longitudinal regions but encompassed all root tissues, the tissue-specific nature of any oscillating transcripts was not captured (Moreno-Risueno et al, 2010).…”

“…In this region of lower auxin levels and response, cell-and tissue-specific auxin distribution and TIR1/AFB-dependent auxin signaling modules result in the induction of auxin-responsive genes, such as GATA23 and LBD16, and the subsequent activation of LRFCs to undergo nuclear migration and asymmetric cell division Goh et al, 2012). Downstream of the TIR1/AFB auxin receptor proteins, a family of transcriptional repressors comprising the AUXIN/INDOLE-3-ACETIC ACID INDUCIBLE (AUX/IAA) proteins are degraded upon auxin perception, leading to auxininduced gene expression (reviewed by Chapman and Estelle, 2009).…”

Quiescent center initiation in the Arabidopsis lateral root primordia is dependent on the SCARECROW transcription factor

“…Later, Malamy and Benfey (1997) performed an extensive analysis of LRP morphogenesis and proposed eight developmental stages (stage I to stage VII and emergence) based on anatomical criteria and these structural milestones have been confirmed in later studies von Wangenheim et al, 2016). In summary, LRP formation is initiated when asymmetric anticlinal cell divisions of founder cells produce pairs of abutting small cells flanked by longer cells (stage I; Goh et al, 2012). Next, the central smaller cells undergo three further rounds of periclinal cell divisions to create a four-layered primordium (stages II to IV).…”