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...

C4 photosynthesis outperforms the ancestral C3 state in a wide range of natural and agro-ecosystems by affording higher water-use and nitrogen-use efficiencies. It therefore represents a prime target for engineering novel, high-yielding crops by introducing the trait into C3 backgrounds. However, the genetic architecture of C4 photosynthesis remains largely unknown. To define the divergence in gene expression modules between C3 and C4 photosynthesis during leaf ontogeny, we generated comprehensive transcriptome atlases of two Cleomaceae species, Gynandropsis gynandra (C4) and Tarenaya hassleriana (C3), by RNA sequencing. Overall, the gene expression profiles appear remarkably similar between the C3 and C4 species. We found that known C4 genes were recruited to photosynthesis from different expression domains in C3, including typical housekeeping gene expression patterns in various tissues as well as individual heterotrophic tissues. Furthermore, we identified a structure-related module recruited from the C3 root. Comparison of gene expression patterns with anatomy during leaf ontogeny provided insight into genetic features of Kranz anatomy. Altered expression of developmental factors and cell cycle genes is associated with a higher degree of endoreduplication in enlarged C4 bundle sheath cells. A delay in mesophyll differentiation apparent both in the leaf anatomy and the transcriptome allows for extended vein formation in the C4 leaf.

The anaphase-promoting complex/cyclosome (APC/C) is a multisubunit ubiquitin ligase that regulates progression through the cell cycle by marking key cell division proteins for destruction. To ensure correct cell cycle progression, accurate timing of APC/C activity is important, which is obtained through its association with both activating and inhibitory subunits. However, although the APC/C is highly conserved among eukaryotes, no APC/C inhibitors are known in plants. Recently, we have identified ULTRAVIOLET-B-INSENSITIVE4 (UVI4) as a plant-specific component of the APC/C. Here, we demonstrate that UVI4 uses conserved APC/C interaction motifs to counteract the activity of the CELL CYCLE SWITCH52 A1 (CCS52A1) activator subunit, inhibiting the turnover of the A-type cyclin CYCA2;3. UVI4 is expressed in an S phase-dependent fashion, likely through the action of E2F transcription factors. Correspondingly, uvi4 mutant plants failed to accumulate CYCA2;3 during the S phase and prematurely exited the cell cycle, triggering the onset of the endocycle. We conclude that UVI4 regulates the temporal inactivation of APC/C during DNA replication, allowing CYCA2;3 to accumulate above the level required for entering mitosis, and thereby regulates the meristem size and plant growth rate.

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Because of their sessile life style, plants have evolved the ability to adjust to environmentally harsh conditions. An important aspect of stress adaptation involves the reprogramming of the cell cycle to ensure optimal growth. The atypical E2F transcription factor DP-E2F-like 1 (E2Fe/DEL1) had been found previously to be an important regulator of the endocycle onset. Here, a novel role for E2Fe/DEL1 was identified as a transcriptional repressor of the type-II cyclobutane pyrimidine dimerphotolyase DNA repair gene PHR1. Upon ultraviolet-B (UV-B) treatment, plants knocked out for E2Fe/DEL1 had improved DNA repair abilities when compared with control plants, whereas those overexpressing it performed less well. Better DNA repair allowed E2Fe/DEL1 knockout plants to resume endoreduplication faster than control plants, contributing in this manner to UV-B radiation resistance by compensating the stress-induced reduction in cell number by ploidy-dependent cell growth. As E2Fe/ DEL1 levels decreased upon UV-B treatment, we hypothesize that the coordinated transcriptional induction of PHR1 with the endoreduplication onset contributes to the adaptation of plants exposed to UV-B stress.

The quiescent center (QC) of the Arabidopsis (Arabidopsis thaliana) root meristem acts as an organiser that promotes stem cell fate in adjacent cells and patterns the surrounding stem cell niche. The stem cells distal from the QC, the columella stem cells (CSCs), are maintained in an undifferentiated state by the QC-expressed transcription factor WUSCHEL RELATED HOMEOBOX 5 (WOX5) and give rise to the columella cells (CCs). Differentiated CCs provide a feedback signal via secretion of the peptide CLAVATA3/ESR-RELATED 40 (CLE40), which acts through the receptor kinases ARABIDOPSIS CRINKLY4 (ACR4) and CLAVATA1 (CLV1) to control WOX5 expression. Previously, WOX5 protein movement from the QC into CSCs was proposed to be required for CSC maintenance, and the CLE40/CLV1/ACR4 signalling module was suggested to restrict WOX5 mobility or function. Here, these assumptions were tested by exploring the function of CLE40/CLV1/ACR4 in CSC maintenance. However, no role for CLE40/CLV1/ACR4 in constricting the mobility of WOX5 or other fluorescent test proteins was identified. Furthermore, in contrast to previous observations, WOX5 mobility was not required to inhibit CSC differentiation. We propose that WOX5 acts mainly in the QC, where other short-range signals are generated that not only inhibit differentiation but also promote stem cell division in adjacent cells. Therefore, the main function of columella-derived CLE40 signal is to position the QC at a defined distance from the root tip by repressing QC-specific gene expression via the ACR4/CLV1 receptors in the distal domain and by promoting WOX5 expression via the CLV2 receptor in the proximal meristem.

Endoreduplication represents a variation on the cell cycle in which multiple rounds of DNA replication occur without subsequent chromosome separation and cytokinesis, thereby increasing the cellular DNA content. It is known that the DNA ploidy level of cells is controlled by external stimuli such as light; however, limited knowledge is available on how environmental signals regulate the endoreduplication cycle at the molecular level. Previously, we had demonstrated that the conversion from a mitotic cell cycle into an endoreduplication cycle is controlled by the atypical E2F transcription factor, DP-E2F-LIKE1 (DEL1), that represses the endocycle onset. Here, the Arabidopsis (Arabidopsis thaliana) DEL1 gene was identified as a transcriptional target of the classical E2Fb and E2Fc transcription factors that antagonistically control its transcript levels through competition for a single E2F cis-acting binding site. In accordance with the reported opposite effects of light on the protein levels of E2Fb and E2Fc, DEL1 transcription depended on the light regime. Strikingly, modified DEL1 expression levels uncoupled the link between light and endoreduplication in hypocotyls, implying that DEL1 acts as a regulatory connection between endocycle control and the photomorphogenic response.Plant development occurs mostly postembryonically. It involves the production of new cells that arise at the meristems from divisions of pluripotent stem cells, followed by their successive cell cycle exit and differentiation. Due to their sessile life style, plants are exposed to changing environmental conditions and thus are continuously forced to adapt their body plan (Walter et al., 2009;Skirycz and Inzé, 2010). This plasticity requires a close connection between cell division, differentiation, and development. Several studies indicate that the core cell cycle machinery is a direct target of various developmental factors (Gutierrez, 2005;Ramirez-Parra et al., 2005;Busov et al., 2008). Correspondingly, cell division rates and cell cycle gene expression levels change upon biotic and abiotic stresses (Burssens et al., 2000;Granier et al., 2000;Kadota et al., 2004;West et al., 2004). The importance of cell cycle control during plant development is further demonstrated by the aberrant plant morphologies that result from alterations in cell cycle regulation (De Veylder et al., 2001;Wyrzykowska et al., 2002;Dewitte et al., 2003Dewitte et al., , 2007.Over the last decades, the core cell cycle machinery has been well characterized. Upon cell cycle stimulation, cyclin-dependent kinases (CDKs) are activated that in turn relieve the repressive action of the RETINO-BLASTOMA-RELATED (RBR) protein on the E2F transcription factors (Inzé and De Veylder, 2006;Berckmans and De Veylder, 2009), resulting in the transcriptional activation of hundreds of E2F target genes, which are mostly DNA replication genes (Vlieghe et al., 2003;Vandepoele et al., 2005;de Jager et al., 2009;Naouar et al., 2009). The E2F/dimerization partner (DP)/RBR pathway is highly cons...