Auxin-Dependent Cell Cycle Reactivation through Transcriptional Regulation ofArabidopsis E2Faby Lateral Organ Boundary Proteins

Abstract

Multicellular organisms depend on cell production, cell fate specification, and correct patterning to shape their adult body. In plants, auxin plays a prominent role in the timely coordination of these different cellular processes. A well-studied example is lateral root initiation, in which auxin triggers founder cell specification and cell cycle activation of xylem polepositioned pericycle cells. Here, we report that the E2Fa transcription factor of Arabidopsis thaliana is an essential component that regulates the asymmetric cell division marking lateral root initiation. Moreover, we demonstrate that E2Fa expression is regulated by the LATERAL ORGAN BOUNDARY DOMAIN18/LATERAL ORGAN BOUNDARY DOMAIN33 (LBD18/ LBD33) dimer that is, in turn, regulated by the auxin signaling pathway. LBD18/LBD33 mediates lateral root organogenesis through E2Fa transcriptional activation, whereas E2Fa expression under control of the LBD18 promoter eliminates the need for LBD18. Besides lateral root initiation, vascular patterning is disrupted in E2Fa knockout plants, similarly as it is affected in auxin signaling and lbd mutants, indicating that the transcriptional induction of E2Fa through LBDs represents a general mechanism for auxin-dependent cell cycle activation. Our data illustrate how a conserved mechanism driving cell cycle entry has been adapted evolutionarily to connect auxin signaling with control of processes determining plant architecture. INTRODUCTIONAs plants develop postembryonically, they produce continuously new structures in a flexible manner, allowing modifications in plant architecture in response to environmental conditions and specific needs. To model the body plan in accordance with external triggers, plant hormones, in particular auxin, play an important role (Friml, 2003;Tanaka et al., 2006;Vanneste and Friml, 2009). Auxin maxima can be found at organ initiation sites as well as in organs upon, for instance, gravity or light stimuli (Friml et al., 2002;Benková et al., 2003;Fuchs et al., 2003;Esmon et al., 2006;Traas and Moné ger, 2010). A well-studied example of hormone-driven morphogenesis is root architecture that is determined by the number and placement of lateral roots (Overvoorde et al., 2010). In Arabidopsis thaliana, lateral root initiation is preceded by an oscillating auxin response in the basal meristem, priming the xylem-pole pericycle (XPP) as founder cells of lateral root primordia (De Smet et al., 2007;De Rybel et al., 2010;Moreno-Risueno et al., 2010). As they mature, these cells have the potential to undergo an asymmetric cell division, initiating the formation of a new lateral root. The subsequent cell divisions follow a well-organized pattern, resulting in lateral root emergence (Pé ret et al., 2009).The molecular mechanism controlling lateral root initiation is based on the auxin-dependent degradation of INDOLE-ACETIC ACID INDUCED PROTEIN14 (IAA14)/SOLITARY ROOT (SLR), which leads to the derepression of AUXIN RESPONSE FACTOR7 (ARF7) and ARF19 (Fukaki et al., 2002;Okushima et al., 2005;Wilm...

Transcriptome Profiling of Tiller Buds Provides New Insights into PhyB Regulation of Tillering and Indeterminate Growth in Sorghum

“…In Arabidopsis, AtE2FA is required for lateral root initiation and vascular patterning (Berckmans et al, 2011).…”

Lateral root emergence in Arabidopsis is dependent on transcription factor LBD29 regulating auxin influx carrier LAX3

“…During LR initiation, LBD16 has been shown to play an important role promoting asymmetric cell division of LR founder cells, controlling polarized nuclear migration to the common cell pole between pairs of founder cells (Goh et al, 2012). LBD18 and LBD33 positively regulate the cell cycle via the transcriptional regulation of E2Fa (Berckmans et al, 2011). LBD29 has also been reported to be involved in the regulation of the cell cycle progression during LR formation (Feng et al, 2012).…”

“…Several LBD proteins have been reported to interact with other family members or distinct classes of transcription factors that may help confer target specificity. For example, LBD18 and LBD33 dimerize to regulate cell cycle by activating E2FA transcription during LR initiation (Berckmans et al, 2011) and LBD6 (AtAS2) interacts with a MYB transcription factor AtAS1 during leaf development (Xu et al, 2003). In summary, LBD family members play key regulatory roles throughout plant development, including LBD16, LBD18 and LBD29, which are critical for LR development.…”

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

“…Among the LBDs-SRDX that we tested, LBD16-SRDX inhibits LR initiation most efficiently, strongly suggesting that LBD16/ASL18 is one of the key regulators for ACDs of the LR founder cells ( Recently, Berckmans et al (Berckmans et al, 2011) reported that LBD18/ASL20 and LBD33/ASL24 function as a heterodimer and regulate the cell cycle reactivation on LR initiation through transcriptional activation of cell cycle controller, E2Fa (Berckmans et al, 2011). LBD18/ASL20 is also involved in the LR primordium development and emergence (Lee et al, 2009), as well as in the xylem tissue differentiation (Soyano et al, 2008).…”