The Plant-Specific Cyclin-Dependent Kinase CDKB1;1 and Transcription Factor E2Fa-DPa Control the Balance of Mitotically Dividing and Endoreduplicating Cells in Arabidopsis

Boudolf, Véronique; Vlieghe, Kobe; Beemster, Gerrit T.S.; Magyar, Zoltán; Acosta, Juan Antonio Torres; Maes, Sara; Schueren, Els Van Der; Inzé, Dirk; Veylder, Lieven De

doi:10.1105/tpc.104.024398

Cited by 266 publications

(279 citation statements)

References 53 publications

(52 reference statements)

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“…Recent genetic evidence strongly supports the classical ''karyoplasmic ratio'' theory that one mechanism to increase cell size is by increasing the ploidy level within a cell, for example through endoreduplication, defined as the amplification of chromosomal DNA without corresponding cell division (3). Several mutants and transgenic plants that have aberrant levels of endoreduplication have been isolated and have led to the identification of key regulators of the endoreduplication cycle or endocycle (3)(4)(5)(6)(7). How these regulators control downstream events, however, remains to be elucidated.…”

mentioning

confidence: 95%

RHL1 is an essential component of the plant DNA topoisomerase VI complex and is required for ploidy-dependent cell growth

Sugimoto‐Shirasu

Roberts

Stacey

et al. 2005

Proc. Natl. Acad. Sci. U.S.A.

111

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How cells achieve their final sizes is a pervasive biological question. One strategy to increase cell size is for the cell to amplify its chromosomal DNA content through endoreduplication cycles. Although endoreduplication is widespread in eukaryotes, we know very little about its molecular mechanisms. Successful progression of the endoreduplication cycle in Arabidopsis requires a plant homologue of archaeal DNA topoisomerase (topo) VI. To further understand how DNA is endoreduplicated and how this process is regulated, we isolated a dwarf Arabidopsis mutant, hyp7 (hypocotyl 7), in which various large cell types that in the wild type normally endoreduplicate multiple times complete only the first two rounds of endoreduplication and stall at 8C. HYP7 encodes the RHL1 (ROOT HAIRLESS 1) protein, and sequence analysis reveals that RHL1 has similarity to the C-terminal domain of mammalian DNA topo II␣, another type II topo that shares little sequence homology with topo VI. RHL1 shows DNA binding activity in vitro, and we present both genetic and in vivo evidence that RHL1 forms a multiprotein complex with plant topo VI. We propose that RHL1 plays an essential role in the topo VI complex to modulate its function and that the two distantly related topos, topo II and topo VI, have evolved a common domain that extends their function. Our data suggest that plant topo II and topo VI play distinct but overlapping roles during the mitotic cell cycle and endoreduplication cycle.endoreduplication ͉ hypocotyl ͉ root hairless T he control of cell size is a highly regulated process with inputs from genetic, hormonal, and environmental cues. Yeast and mammalian cells usually only double their size during their development; therefore, a key question in their size control is how proliferating cells coordinate cell growth and cell division to maintain size homeostasis. Yeast and many mammalian cells have a cell size checkpoint mechanism in which cells divide only when they reach a critical size (1), whereas some mammalian cells may control their size through extracellular signals (2). Although plant cells also double their cell size during proliferation, they commonly undergo an additional, massive (sometimes Ͼ1,000-fold), postmitotic cell enlargement. Such a large increase in volume is driven by a combination of production of new cytoplasmic mass and cell expansion (driven by water uptake and vacuolar growth), but little is known about the underlying mechanisms involved. Recent genetic evidence strongly supports the classical ''karyoplasmic ratio'' theory that one mechanism to increase cell size is by increasing the ploidy level within a cell, for example through endoreduplication, defined as the amplification of chromosomal DNA without corresponding cell division (3). Several mutants and transgenic plants that have aberrant levels of endoreduplication have been isolated and have led to the identification of key regulators of the endoreduplication cycle or endocycle (3-7). How these regulators control downstream events, however, rem...

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mentioning

confidence: 95%

RHL1 is an essential component of the plant DNA topoisomerase VI complex and is required for ploidy-dependent cell growth

Sugimoto‐Shirasu

Roberts

Stacey

et al. 2005

Proc. Natl. Acad. Sci. U.S.A.

111

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“…For example, inhibition of CDKA activity at the G2-to-M transition by low overproduction levels of Kip-related protein 2 caused cells to enter prematurely into the endocycle (Verkest et al, 2005). Similarly, downregulation of CDKB1;1 activity by ectopic expression of its dominant-negative variant enhanced endoreduplication (Boudolf et al, 2004b). Thus, the enhanced level of endoreduplication in the hub1-1 mutant probably resulted from the block in the G2-to-M transition suggested by flow cytometry data in combination with ongoing G1-to-S activity.…”

Section: Hub1 Affects G2-to-m Transition and Mitosismentioning

confidence: 99%

TheArabidopsis thalianaHomolog of YeastBRE1Has a Function in Cell Cycle Regulation during Early Leaf and Root Growth

et al. 2007

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Chromatin modification and transcriptional activation are novel roles for E3 ubiquitin ligase proteins that have been mainly associated with ubiquitin-dependent proteolysis. We identified HISTONE MONOUBIQUITINATION1 (HUB1) (and its homolog HUB2) in Arabidopsis thaliana as RING E3 ligase proteins with a function in organ growth. We show that HUB1 is a functional homolog of the human and yeast BRE1 proteins because it monoubiquitinated histone H2B in an in vitro assay. Hub knockdown mutants had pale leaf coloration, modified leaf shape, reduced rosette biomass, and inhibited primary root growth. One of the alleles had been designated previously as ang4-1. Kinematic analysis of leaf and root growth together with flow cytometry revealed defects in cell cycle activities. The hub1-1 (ang4-1) mutation increased cell cycle duration in young leaves and caused an early entry into the endocycles. Transcript profiling of shoot apical tissues of hub1-1 (ang4-1) indicated that key regulators of the G2-to-M transition were misexpressed. Based on the mutant characterization, we postulate that HUB1 mediates gene activation and cell cycle regulation probably through chromatin modifications.

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“…The J0121 and J0661 lines (Laplaze et al, 2005) were used to locate pericycle-like cells during rooting. The following mutant lines were used: wol-1 (Scheres et al, 1995), ahp1 ahp2 ahp3 (Hutchison et al, 2006), ahp2 ahp4 ahp5, arr1 arr10 arr12 (Mason et al, 2005), aux1-22 (Bennett et al, 1996), axr2-1 (Timpte et al, 1994), slr-1 (Fukaki et al, 2005), crane-2 (Uehara et al, 2008), sur2-1 (Delarue et al, 1998), and iaa28-1 (Rogg et al, 2001), which were obtained from NASC; and pin1, pin2 pin3, pin2 pin3 pin7 (Blilou et al, 2005), fwr (Okumura et al, 2013), cyclinb1;1 (cycb1;1) and cycb1;2 (Nowack et al, 2012), and CDKB1;1 DN161 and Pro 35S :KRP2 (Boudolf et al, 2004;Verkest et al, 2005). We also used the following stem cell niche mutants: blj-1 jkd-4 scr-4 (MorenoRisueno et al, 2015), scr-4 (Fukaki et al, 1996), shr-2 Pro SHR :SHR:GR (Levesque et al, 2006), plt1-4 plt2-2 (Aida et al, 2004), jkd-4 (Welch et al, 2007, scz-1 (Mylona et al, 2002), and wox5-1 (Sarkar et al, 2007), and jkd-4 scz-1 and shr-2 plt1-4 plt2-2 Pro SHR :SHR:GR (generated in this study).…”

Section: Plant Materialsmentioning

confidence: 99%

Regulation of Hormonal Control, Cell Reprogramming, and Patterning during De Novo Root Organogenesis

et al. 2017

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Body regeneration through formation of new organs is a major question in developmental biology. We investigated de novo root formation using whole leaves of Arabidopsis (Arabidopsis thaliana). Our results show that local cytokinin biosynthesis and auxin biosynthesis in the leaf blade followed by auxin long-distance transport to the petiole leads to proliferation of J0121-marked xylem-associated tissues and others through signaling of INDOLE-3-ACETIC ACID INDUCIBLE28 (IAA28), CRANE (IAA18), WOODEN LEG, and ARABIDOPSIS RESPONSE REGULATORS1 (ARR1), ARR10, and ARR12. Vasculature proliferation also involves the cell cycle regulator KIP-RELATED PROTEIN2 and ABERRANT LATERAL ROOT FORMATION4, resulting in a mass of cells with rooting competence that resembles callus formation. Endogenous callus formation precedes specification of postembryonic root founder cells, from which roots are initiated through the activity of SHORT-ROOT, PLETHORA1 (PLT1), and PLT2. Primordia initiation is blocked in shr plt1 plt2 mutant. Stem cell regulators SCHIZORIZA, JACKDAW, BLUEJAY, and SCARECROW also participate in root initiation and are required to pattern the new organ, as mutants show disorganized and reduced number of layers and tissue initials resulting in reduced rooting. Our work provides an organ regeneration model through de novo root formation, stating key stages and the primary pathways involved.Plants have striking regeneration capacities, and can produce new organs from postembryonic tissues (Hartmann et al., 2010;Chen et al., 2014;Liu et al., 2014) as well as reconstitute damaged organs upon wounding (Xu et al., 2006;Heyman et al., 2013; PerianezRodriguez et al., 2014;Melnyk et al., 2015;Efroni et al., 2016). Intriguingly, root regeneration upon stem cell damage recruits embryonic pathways (Hayashi et al., 2006;Efroni et al., 2016), whereas in contrast, postembryonic formation of whole new organs, such as lateral roots, appears to use specific postembryonic pathways (Lavenus et al., 2013).Cross talk between auxin and cytokinin signaling is required for many aspects of plant development and regeneration (El-Showk et al., 2013), although how their synergistic interaction is implemented at the molecular level has not been clarified (Skoog and Miller, 1957;Chandler and Werr, 2015). Exogenous in vitro supplementation of these two hormones results in continuous cell proliferation, to form a characteristic structure termed "callus". Callus emerges as a common regenerative mechanism for almost all plant organs through in vitro culture (Atta et al., 2009;Sugimoto et al., 2010). There is increasing evidence that callus formation requires hormone-mediated activation of a lateral and meristematic root development program in pericycle-like cells defined by expression of the J0121 marker 1 This work was supported by grants from Ministerio de Economía y Competitividad (MINECO) of Spain, the European Regional Development Fund (ERDF) and FP7 Funds of the European Commission, BFU2013-41160-P, BFU2016-80315-P, and PCIG11-GA-2012-322082 to M.A....

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The Plant-Specific Cyclin-Dependent Kinase CDKB1;1 and Transcription Factor E2Fa-DPa Control the Balance of Mitotically Dividing and Endoreduplicating Cells in Arabidopsis

Cited by 266 publications

References 53 publications

RHL1 is an essential component of the plant DNA topoisomerase VI complex and is required for ploidy-dependent cell growth

RHL1 is an essential component of the plant DNA topoisomerase VI complex and is required for ploidy-dependent cell growth

TheArabidopsis thalianaHomolog of YeastBRE1Has a Function in Cell Cycle Regulation during Early Leaf and Root Growth

Regulation of Hormonal Control, Cell Reprogramming, and Patterning during De Novo Root Organogenesis

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