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First published online December 31, 2008; 10.1104/pp.108.131797 Plant Physiology 149:1387-1398 (2009) © 2009 American Society of Plant Biologists OPEN ACCESS ARTICLE
Eternal Youth, the Fate of Developing Arabidopsis Leaves upon Rhodococcus fascians Infection1,[C],[W],[OA]Department of Plant Systems Biology, Flanders Institute for Biotechnology, and Department of Plant Biotechnology and Genetics, Ghent University, 9052 Ghent, Belgium
The phytopathogenic actinomycete Rhodococcus fascians induces neoplastic shooty outgrowths on infected hosts. Upon R. fascians infection of Arabidopsis (Arabidopsis thaliana), leaves are formed with small narrow lamina and serrated margins. These symptomatic leaves exhibit reduced tissue differentiation, display more but smaller cells that do not endoreduplicate, and accumulate in the G1 phase of the cell cycle. Together, these features imply that leaf growth occurs primarily through mitotic cell division and not via cell expansion. Molecular analysis revealed that cell cycle gene expression is activated continuously throughout symptomatic leaf development, ensuring persistent mitotic cycling and inhibition of cell cycle exit. The transition at the two major cell cycle checkpoints is stimulated as a direct consequence of the R. fascians signals. The extremely reduced phenotypical response of a cyclind3;1-3 triple knockout mutant indicates that the D-type cyclin/retinoblastoma/E2F transcription factor pathway, as a major mediator of cell growth and cell cycle progression, plays a key role in symptom development and is instrumental for the sustained G1-to-S and G2-to-M transitions during symptomatic leaf growth.
The Gram-positive phytopathogenic bacterium Rhodococcus fascians secretes growth-modulating hormones, such as cytokinins and auxins, and typically induces neoplastic, shooty outgrowths on a wide range of plant hosts (Goethals et al., 2001  ; Putnam and Miller, 2007). Whereas the role of auxin production in the symptomatology remains to be determined (Vandeputte et al., 2005), the central position of cytokinin secretion has been clearly established (Crespi et al., 1992, 1994; Temmerman et al., 2000; Pertry et al., 2009). The proliferation of shooty tissue in tobacco (Nicotiana tabacum) not only relies on activation of existing (dormant) meristems but also on de novo meristem formation in cortical tissues by reactivation of the cell cycle, a process that is accompanied by expression of the cyclins CYCB1;1 and CYCD3;2 (de O Manes et al., 2001). In Arabidopsis (Arabidopsis thaliana), only newly formed organs become symptomatic upon R. fascians infection. A strong induction of CYCA2;1 expression, followed by an enhanced transcription of CYCB1;1 and the cyclin-dependent kinase CDKA;1 upon infection, illustrates activation of the cell cycle in this host (Vereecke et al., 2000).
Plants can rapidly alter their growth rate and pattern in response to developmental and external conditions (Traas et al., 1998
Cell cycle control and plant development are mainly integrated at the cell cycle checkpoints (G1/S and G2/M) and the molecular machineries involved (De Veylder et al., 2003 Here, we analyzed the development of newly formed symptomatic leaves in Arabidopsis upon infection with R. fascians and asked how modulation of the plant cell cycle is involved in symptom establishment. Our data show that the bacterial signals directly stimulate progression at the G1/S and G2/M checkpoints, which commits the leaf cells to mitotic cycling. Consequently, symptomatic leaves never reach maturity and are blocked in a physiological state that is relevant for niche establishment.
R. fascians Infection Inhibits Leaf Differentiation
Typically, infection of Arabidopsis plants with the wild-type R. fascians strain D188 generates symptomatic leaves with small and narrow leaf blades and strongly serrated margins (Depuydt et al., 2008
Altogether, these observations suggest that cell proliferation is the dominant mechanism for growth in symptomatic leaves and that differentiation is impaired. The latter was confirmed by microscopic analysis of cross-sections through the lamina (Fig. 2, A and B ). Indeed, all of the parenchyma cells of D188-infected leaves were spherical with fewer intercellular air spaces than in control leaves, making it difficult to distinguish the palisade and spongy mesophyll layers (Fig. 2).
R. fascians Prevents Endocycling during Leaf Development
The data above indicate that the balance between cell proliferation and cell differentiation is disturbed during leaf maturation upon infection with R. fascians strain D188. In a time course experiment, we examined the endoreduplication kinetics as a marker for cell differentiation. Infections were carried out as described above, and together with leaf 5, the next three emerging leaves were analyzed at 3, 7, 10, 14, 16, 19, and 24 dpi (Fig. 3
). Hence, four different stages in leaf development were considered: outgrowing primordia and young, expanding, and mature leaves. For leaves 5 and 6, no significant differences between the two conditions were measured, which was anticipated because of the lack of morphological alterations in these leaves (Depuydt et al., 2008
Maintenance of High Transcription Levels of Mitotic Cell Cycle Genes throughout Symptomatic Leaf Development Imposes a Commitment to Mitotic Cycling
Most cells (60%–65%) in symptomatic leaves have a 2C content, implying that infection with R. fascians promotes the G2-to-M transition. Since CDKB1;1 expression typically correlates with proliferating cells and plays a key role at the G2/M checkpoint, the expression pattern of CDKB1;1 was analyzed upon infection with R. fascians. Histochemical analyses of CDKB1;1:GUS marker lines revealed promoter activity throughout the lamina of symptomatic leaves. The reported typical stomatal expression (Boudolf et al., 2004a
Expression of CDKA;1 and CYCA2;3, as a complex involved in the negative regulation of endocycling (Imai et al., 2006 ), was also specifically down-regulated as control leaves differentiated (Fig. 5, A and B
). Interestingly, upon infection with D188, a biphasic expression pattern reminiscent of that of CDKB1;1 was observed for both genes (Fig. 5, A and B), confirming the proliferative status of symptomatic leaves. A similar differential expression in control versus infected leaves of E2Fe/DEL1 (Fig. 5C), exclusively present in mitotically dividing cells (Vlieghe et al., 2005; Lammens et al., 2008), together with the expansion of the expression zone in infected E2Fe/DEL1:GUS leaves beyond the leaf base into the leaf blade (Fig. 5, D and E), further support that leaf growth is only driven by mitotic cell divisions upon R. fascians infection.
Infection and subsequent determination of the disease phenotype and ploidy level distribution in symptomatic leaves of ccs52a2 and del1-1 knockout plants and in plants overexpressing E2Fe/DEL1 or SIM showed that these regulators do not play a significant role in the increased CDK activity and the stimulated progression at the G2-to-M transition during symptom development (Supplemental Fig. S1), suggesting that CDK expression and/or activity might be directly targeted by the R. fascians signals.
The continuation of mitotic cell divisions during symptomatic leaf development implies that cells not only efficiently pass the G2-to-M transition but subsequently cross the G1/S checkpoint and enter the S phase of the cell cycle. Entry into the S phase involves RBR phosphorylation and subsequent activation of S-phase gene expression in a CYCD3-dependent way (De Veylder et al., 2002
These data suggested that the CYCD3/RBR/E2F-DP pathway might be modulated upon R. fascians infection by direct targeting of the CYCD3 genes. The strongly reduced response of a cycd3;1-3 triple mutant line confirmed this hypothesis (Table I; Fig. 7 ). Importantly, in the triple mutant, the most typical aspects of the symptomatology were much less pronounced: activation of axillary meristems was only observed in 7% of the infected plants (versus 67% in wild-type plants), and leaves with serrated margins were not observed (versus 95% in wild-type plants). Leaf expansion was impaired upon infection, but not to the same extent as in infected wild-type plants (Fig. 7). The epidermal pavement cells of the infected triple mutant were sinusoid rather than polygon shaped, and their size was intermediate between the cycd3;1-3 controls and infected wild-type plants (Fig. 7). Flow cytometric analysis during development of leaf 8 of the noninfected cycd3;1-3 triple mutant revealed an initially higher level of cells with a 4C content and an earlier and steeper increase of cells with an 8C content (Fig. 8A ) than in noninfected wild-type leaves (Fig. 3), confirming the premature onset of endoreduplication (Dewitte et al., 2007 ). In contrast to the effect on wild-type plants (Fig. 3), infection with D188 did not result in the typically high proportion of cells with a 2C content during development of leaf 8 of the cycd3;1-3 mutant, indicating that the activation of CYCD3 expression upon infection is required for the preclusion of endocycle onset. Interestingly, the number of cells with an 8C content decreased over time and was finally half that of the controls, suggesting that the R. fascians signals can still interfere with endoreduplication in the cycd3;1-3 mutant plants. The intermediate response of cycd3;1-3 plants to R. fascians infection could also be demonstrated at the molecular level by assessing the expression of marker genes (Depuydt et al., 2008). In agreement with the absence of leaf margin serrations, no ectopic expression of SHOOT MERISTEMLESS (STM), a meristem-associated class I KNOX gene, could be observed (Table I), but cytokinin signaling was still activated, as indicated by enhanced ARABIDOPSIS RESPONSE REGULATOR5 (ARR5) expression. Moreover, induced expression of E2Fe/DEL1 and CDKB1;1 and down-regulation of RBR were maintained in the infected cycd3;1-3 triple mutants. Nevertheless, the differential expression levels were much lower than those of infected wild-type controls (Table I).
As described above, CYCD3;1OE plants had features that resembled R. fascians-induced phenotypes. Interestingly, these transgenic lines were only partially responsive to infection. Whereas axillary meristems were activated as in wild-type plants, leaf expansion was only partially compromised, no leaf serrations were observed (Fig. 7A), and the very small epidermal pavement cell size of the CYCD3;1OE plants was not further reduced upon infection (Fig. 7B). Moreover, the DNA ploidy level distribution did not change upon infection, no high population of cells with a 2C content could be established (Fig. 8D), and no differential expression of the marker genes was detected (Table I).
Arabidopsis leaves that develop upon infection with R. fascians strain D188 have a typical small and narrow leaf blade and serrated margins. The latter is accomplished by ectopic expression of meristem-associated class I KNOX genes, but the cause for the strongly reduced leaf expansion had not been addressed (Depuydt et al., 2008 ). Here, we determined that the small lamina size is caused by an almost 5-fold reduction in cell size that could not be compensated for by the 2- to 3-fold increase in cell number. The increased number of meristemoids, the reduced tissue differentiation, and the very high level of cells with a 2C content all illustrate that cells in D188-infected leaves hardly differentiate and remain in the proliferative state. These data imply that the time window in which mitotic cell division drives leaf growth is greatly extended upon infection and, moreover, indicate that, in symptomatic leaves, the subsequent stage of leaf growth via cell expansion, driven by endoreduplication, is never attained.
An increase in cell cycle gene expression upon infection with R. fascians had been reported previously in tobacco and Arabidopsis plants. Outer cortical cells of infected tobacco plants reenter the cell cycle, and subsequent divisions result in the formation of shoot primordia. The reiteration of this process together with the activation of axillary meristems ultimately culminates in the typical leafy gall symptom on tobacco and is correlated with the up-regulation of CYCD3;2 and CYCB1;1 (de O Manes et al., 2001
The persistent expression of the mitotic CDKs, CDKB1;1 and CDKA;1, and of CYCA2;3 continues to promote the G2-to-M transition. A fast progression through mitosis had been observed in tobacco Bright Yellow 2 cell cultures infected with R. fascians that was accompanied with transcriptional activation of genes associated with the G2/M phase (Vandeputte et al., 2007
The transcriptional analysis indicated that the CYCD3/RBR/E2F-DP pathway that controls the G1-to-S transition was also modulated. Indeed, RBR expression was down-regulated upon infection, and all three CYCD3 genes were significantly up-regulated throughout development of the infected leaves. The CYCD3 proteins function as growth factor sensors (Riou-Khamlichi et al., 1999
Although transgenic CYCD3;1OE plants exhibit features that are reminiscent of R. fascians-induced symptoms, the overall phenotype was very different from that of infected wild-type plants. Indeed, expression of CYCD3;1 from the 35S promoter does not affect the overall organ size. More importantly, in contrast to R. fascians-infected plants in which cells accumulate in the G1 phase, the strongly enhanced G1-to-S transition is not accompanied with a promotion of the G2-to-M transition; hence, cells accumulate in the G2 phase (Dewitte et al., 2003
In conclusion, our data demonstrate that R. fascians modulates plant development by manipulating both checkpoints of the cell cycle (Fig. 9
). Upon infection, the fast G1-to-S transition is accompanied by a fast G2-to-M transition; thus, most cells of symptomatic leaves are in the G1 phase. CYCD3 activity plays a central role in symptom development and potentially mediates both transitions, although direct targeting of CDKB1;1 might also contribute to the persistent mitotic cycling of the infected tissues. As a consequence of the action of the bacterial morphogens, newly formed organs only grow through mitotic cell divisions, hardly differentiate, and never reach maturity. It is hypothesized that young dividing tissues would provide the bacteria with specific nutrients that give a selective advantage over other plant-inhabiting microorganisms (Vereecke et al., 2002a
Plant Materials and Growth Conditions
Arabidopsis (Arabidopsis thaliana L. Heyhn.) seeds were germinated and grown on half-strength Murashige and Skoog medium in a growth chamber under a 16-h/8-h light/dark photoperiod at 21°C ± 2°C, after sterilization by submergence for 2 min in 70% ethanol (v/v) and 12 min in 5% (w/v) NaOCl supplemented with 0.1% (v/v) polyoxyethylenesorbitan 20, and rinsing at least five times with sterile water. Unless stated otherwise, wild-type ecotype C24 was used for the infection experiments, obtained from the European Arabidopsis Stock Centre. CYCD3;1OE and cycd3;1-3 lines were obtained from Jim Murray (Dewitte et al., 2003
The Rhodococcus fascians strains used were the pathogenic strain D188, containing the linear virulence plasmid pFiD188 and its plasmid-free nonpathogenic derivative D188-5 (Desomer et al., 1988
The leaf area was determined by photographing the leaf with a binocular MZFLIII (Leica) and analyzing the picture with the public domain image-analysis program ImageJ (http://rsb.info.nig.gov/ij/; version 1.32j). For cell density and cell area, the leaves were cleared overnight in ethanol (70% [v/v]) and stored in lactic acid for analysis on a microscope stage fitted with differential interference contrast optics (DMLB; Leica). Images of at least 30 cells of the abaxial epidermis located at 25% and 75% from the leaf base, halfway between the midrib and the leaf margin, were drawn with a drawing tube mounted on the microscope. These images were scanned and processed with ImageJ. The total number of cells was estimated by dividing the leaf area with the average cell area. At least five independent biological repeats were analyzed, and average data are shown. The total numbers of stomata and meristemoids were derived by extrapolating the number of stomata and meristemoids, identified by cell shape and size, in the drawing tube images to the full leaf surface area.
Depending on the experiment, leaf 5, 6, 7, and/or 8 was sampled (Figs. 3 and 8, A–C) or symptomatic leaves were pooled (Figs. 4, E and F, and 8D; Supplemental Fig. S1). Leaves were chopped with a razor blade in 300 µL of buffer (45 mM MgCl2, 30 mM sodium citrate, 20 mM MOPS, and 1% Triton X-100, pH 7; Galbraith et al., 1991
The GUS assays were done as described (Beeckman and Engler, 1994
For qRT-PCR, leaf 8 was sampled in a time course experiment and stored at –70°C until further processing. RNA was extracted from leaf tissue with the RNeasy kit (Qiagen). cDNA was prepared from 2 µg of total RNA with SuperScript II reverse transcriptase (Invitrogen) according to the manufacturer's instructions. qRT-PCRs were quantified on a Lightcycler480 apparatus (Roche Diagnostics) with SYBR Green for detection in a 5-µL volume (2.5 µL of master, 0.25 µL of 5 µM of each forward and reverse primer, and 2 µL of cDNA) in triplicate on a 384-multiwell plate to allow determination of mean and SD of cycle threshold (CT) values. Data were analyzed with the 2–
The following materials are available in the online version of this article.
We thank Gerrit Beemster for fruitful discussions, Walter Dewitte for critical reading of the manuscript, Martine De Cock for help in preparing it, and Karel Spruyt for photographs. Received October 28, 2008; accepted December 25, 2008; published December 31, 2008.
1 This work was supported by the Bijzonder Onderzoeksfonds of Ghent University (predoctoral fellowship to S.D.).  The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantphysiol.org) is: Danny Vereecke (danny.vereecke{at}psb.ugent.be).
[C] Some figures in this article are displayed in color online but in black and white in the print edition.
[W] The online version of this article contains Web-only data.
[OA] Open Access articles can be viewed online without a subscription. www.plantphysiol.org/cgi/doi/10.1104/pp.108.131797 * Corresponding author; e-mail marcelle.holsters{at}psb.ugent.be.
Beeckman T, Engler G (1994) An easy technique for the clearing of histochemically stained plant tissue. Plant Mol Biol Rep 12: 37–42[CrossRef] Beemster GTS, De Vusser K, De Tavernier E, De Bock K, Inzé D (2002) Variation in growth rate between Arabidopsis ecotypes is correlated with cell division and A-type cyclin-dependent kinase activity. Plant Physiol 129: 854–864 Beemster GTS, Fiorani F, Inzé D (2003) Cell cycle: the key to plant growth control? Trends Plant Sci 8: 154–158[CrossRef][Web of Science][Medline] Boudolf V, Barrôco R, de Almeida Engler J, Verkest A, Beeckman T, Naudts M, Inzé D, De Veylder L (2004a) B1-type cyclin-dependent kinases are essential for the formation of stomatal complexes in Arabidopsis thaliana. Plant Cell 16: 945–955 Boudolf V, Vlieghe K, Beemster GTS, Magyar Z, Torres Acosta JA, Maes S, Van Der Schueren E, Inzé D, De Veylder L (2004b) The plant-specific cyclin-dependent kinase CDKB1;1 and transcription factor E2Fa-DPa control the balance of mitotically dividing and endoreduplicating cells in Arabidopsis. Plant Cell 16: 2683–2692 Boyes DC, Zayed AM, Ascenzi R, McCaskill AJ, Hoffman NE, Davis KR, Görlach J (2001) Growth stage-based phenotypic analysis of Arabidopsis: a model for high throughput functional genomics in plants. Plant Cell 13: 1499–1510 Churchman ML, Brown ML, Kato N, Kirik V, Hülskamp M, Inzé D, De Veylder L, Walker JD, Zheng Z, Oppenheimer DG, et al (2006) SIAMESE, a novel plant-specific cell cycle regulator controls endoreplication onset in Arabidopsis thaliana. Plant Cell 18: 3145–3157 Cionini PG, Cavallini A, Baroncelli S, Lercari B, D'Amato F (1983) Diploidy and chromosome endoreduplication in the development of epidermal cell lines in the first foliage leaf of durum wheat (Triticum durum Desf.). Protoplasma 118: 36–43[CrossRef][Web of Science] Crespi M, Messens E, Caplan AB, Van Montagu M, Desomer J (1992) Fasciation induction by the phytopathogen Rhodococcus fascians depends upon a linear plasmid encoding a cytokinin synthase gene. EMBO J 11: 795–804[Medline] Crespi M, Vereecke D, Temmerman W, Van Montagu M, Desomer J (1994) The fas operon of Rhodococcus fascians encodes new genes required for efficient fasciation of host plants. J Bacteriol 176: 2492–2501 del Pozo JC, Diaz-Trivino S, Cisneros N, Gutierrez C (2006) The balance between cell division and endoreplication depends on E2FC-DPB, transcription factors regulated by the ubiquitin-SCFSKP2A pathway in Arabidopsis. Plant Cell 18: 2224–2235 den Boer BGW, Murray JAH (2000) Control of plant growth and development through manipulation of cell-cycle genes. Curr Opin Biotechnol 11: 138–145[CrossRef][Web of Science][Medline] de O Manes C-L, Beeckman T, Ritsema T, Van Montagu M, Goethals K, Holsters M (2004) Phenotypic alterations in Arabidopsis thaliana plants caused by Rhodococcus fascians infection. J Plant Res 117: 139–145[CrossRef][Medline] de O Manes C-L, Van Montagu M, Prinsen E, Goethals K, Holsters M (2001) De novo cortical cell division triggered by the phytopathogen Rhodococcus fascians in tobacco. Mol Plant Microbe Interact 14: 189–195[Medline] Depuydt S, Dole Depuydt S, Trenkamp S, Fernie AR, Elftieh S, Renou J-P, Vuylsteke M, Holsters M, Vereecke D (2009) An integrated genomics approach to define niche establishment by Rhodococcus fascians. Plant Physiol 149: 1366–1386 Desomer J, Dhaese P, Van Montagu M (1988) Conjugative transfer of cadmium resistance plasmids in Rhodococcus fascians strains. J Bacteriol 170: 2401–2405 De Veylder L, Beeckman T, Beemster GTS, de Almeida Engler J, Ormenese S, Maes S, Naudts M, Van Der Schueren E, Jacqmard A, Engler G, et al (2002) Control of proliferation, endoreduplication and differentiation by the Arabidopsis E2Fa/DPa transcription factor. EMBO J 21: 1360–1368[CrossRef][Web of Science][Medline] De Veylder L, Beeckman T, Beemster GTS, Krols L, Terras F, Landrieu I, Van Der Schueren E, Maes S, Naudts M, Inzé D (2001) Functional analysis of cyclin-dependent kinase inhibitors of Arabidopsis. Plant Cell 13: 1653–1667 De Veylder L, Joubès J, Inzé D (2003) Plant cell cycle transitions. Curr Opin Plant Biol 6: 536–543[CrossRef][Web of Science][Medline] Dewitte W, Murray JAH (2003) The plant cell cycle. Annu Rev Plant Biol 54: 235–264[CrossRef][Medline] Dewitte W, Riou-Khamlichi C, Scofield S, Healy JMS, Jacqmard A, Kilby NJ, Murray JAH (2003) Altered cell cycle distribution, hyperplasia, and inhibited differentiation in Arabidopsis caused by the D-type cyclin CYCD3. Plant Cell 15: 79–92 Dewitte W, Scofield S, Alcasabas AA, Maughan SC, Menges M, Braun N, Collins C, Nieuwland J, Prinsen E, Sundaresan V, et al (2007) Arabidopsis CYCD3 D-type cyclins link cell proliferation and endocycles and are rate-limiting for cytokinin responses. Proc Natl Acad Sci USA 104: 14537–14542 Donnelly PM, Bonetta D, Tsukaya H, Dengler RE, Dengler NG (1999) Cell cycling and cell enlargement in developing leaves of Arabidopsis. Dev Biol 215: 407–419[CrossRef][Web of Science][Medline] Ferjani A, Horiguchi G, Yano S, Tsukaya H (2007) Analysis of leaf development in fugu mutants of Arabidopsis reveals three compensation modes that modulate cell expansion in determinate organs. Plant Physiol 144: 988–999 Francis D, Sorrell DA (2001) The interface between the cell cycle and plant growth regulators: a mini review. Plant Growth Regul 33: 1–12[CrossRef][Web of Science] Galbraith DW, Harkins KR, Knapp S (1991) Systemic endopolyploidy in Arabidopsis thaliana. Plant Physiol 96: 985–989 Gendreau E, Höfte H, Grandjean O, Brown S, Traas J (1998) Phytochrome controls the number of endoreduplication cycles in the Arabidopsis thaliana hypocotyl. Plant J 13: 221–230[CrossRef][Web of Science][Medline] Gendreau E, Orbovic V, Höfte H, Traas J (1999) Gibberellin and ethylene control endoreduplication levels in the Arabidopsis thaliana hypocotyl. Planta 209: 513–516[Web of Science][Medline] Goethals K, Vereecke D, Jaziri M, Van Montagu M, Holsters M (2001) Leafy gall formation by Rhodococcus fascians. Annu Rev Phytopathol 39: 27–52[CrossRef][Web of Science][Medline] Hemerly A, de Almeida Engler J, Bergounioux C, Van Montagu M, Engler G, Inzé D, Ferreira P (1995) Dominant negative mutants of the Cdc2 kinase uncouple cell division from iterative plant development. EMBO J 14: 3925–3936[Web of Science][Medline] Hu Y, Bao F, Li J (2000) Promotive effect of brassinosteroids on cell division involves a distinct CycD3-induction pathway in Arabidopsis. Plant J 24: 693–701[CrossRef][Web of Science][Medline] Imai KK, Ohashi Y, Tsuge T, Yoshizumi T, Matsui M, Oka A, Aoyama T (2006) The A-type cyclin CYCA2;3 is a key regulator of ploidy levels in Arabidopsis endoreduplication. Plant Cell 18: 382–396 Inzé D (2005) Green light for the cell cycle. EMBO J 24: 657–662[CrossRef][Web of Science][Medline] Inzé D, De Veylder L (2006) Cell cycle regulation in plant development. Annu Rev Genet 40: 77–105[CrossRef][Web of Science][Medline] Jasinski S, Riou-Khamlichi C, Roche O, Perennes C, Bergounioux C, Glab N (2002) The CDK inhibitor NtKIS1a is involved in plant development, endoreduplication and restores normal development of cyclin D3;1-overexpressing plants. J Cell Sci 115: 973–982 Joubès J, Phan T-H, Just D, Rothan C, Bergounioux C, Raymond P, Chevalier C (1999) Molecular and biochemical characterization of the involvement of cyclin-dependent kinase A during the early development of tomato fruit. Plant Physiol 121: 857–869 Kondorosi E, Kondorosi A (2004) Endoreduplication and activation of the anaphase-promoting complex during symbiotic cell development. FEBS Lett 567: 152–157[CrossRef][Web of Science][Medline] Kosugi S, Ohashi Y (2003) Constitutive E2F expression in tobacco plants exhibits altered cell cycle control and morphological change in a cell type-specific manner. Plant Physiol 132: 2012–2022 Lammens T, Boudolf V, Kheibarshekan L, Zalmas LP, Gaamouche T, Maes S, Vanstraelen M, Kondorosi E, La Thangue NB, Govaerts W, et al (2008) Atypical E2F activity restrains APC/CCCS52A2 function obligatory for endocycle onset. Proc Natl Acad Sci USA 105: 14721–14726 Laureys F, Dewitte W, Witters E, Van Montagu M, Inzé D, Van Onckelen H (1998) Zeatin is indispensable for the G2-M transition in tobacco BY-2 cells. FEBS Lett 426: 29–32[CrossRef][Web of Science][Medline] Leiva-Neto JT, Grafi G, Sabelli PA, Dante RA, Woo YM, Maddock S, Gordon-Kamm WJ, Larkins BA (2004) A dominant negative mutant of cyclin-dependent kinase A reduces endoreduplication but not cell size or gene expression in maize endosperm. Plant Cell 16: 1854–1869 Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2– Magyar Z, De Veylder L, Atanassova A, Bakó L, Inzé D, Bögre L (2005) The role of the Arabidopsis E2FB transcription factor in regulating auxin-dependent cell division. Plant Cell 17: 2527–2541 Melaragno JE, Mehrotra B, Coleman AW (1993) Relationship between endopolyploidy and cell size in epidermal tissue of Arabidopsis. Plant Cell 5: 1661–1668[Abstract] Menges M, de Jager SM, Gruissem W, Murray JAH (2005) Global analysis of the core cell cycle regulators of Arabidopsis identifies novel genes, reveals multiple and highly specific profiles of expression and provides a coherent model for plant cell cycle control. Plant J 41: 546–566[CrossRef][Web of Science][Medline] Menges M, Samland AK, Planchais S, Murray JAH (2006) The D-type cyclin CYCD3;1 is limiting for the G1-to-S-phase transition in Arabidopsis. Plant Cell 18: 893–906 Nakai T, Kato K, Shinmyo A, Sekine M (2006) Arabidopsis KRPs have distinct inhibitory activity toward cyclin D2-associated kinases, including plant-specific B-type cyclin-dependent kinase. FEBS Lett 580: 336–340[CrossRef][Web of Science][Medline] Nath U, Crawford BCW, Carpenter R, Coen E (2003) Genetic control of surface curvature. Science 299: 1404–1407 Oakenfull EA, Riou-Khamlichi C, Murray JAH (2002) Plant D-type cyclins and the control of G1 progression. Philos Trans R Soc Lond B Biol Sci 357: 749–760 Pertry I, Václavíková K, Depuydt S, Galuszka P, Spíchal L, Temmerman W, Stes E, Schmülling T, Kakimoto T, Van Montagu M, et al (2009) Identification of Rhodococcus fascians cytokinins and their modus operandi to reshape the plant. Proc Natl Acad Sci USA 106: 929–934 Pettkó-Szandtner A, Mészáros T, Horváth GV, Bakó L, Csordás-Tóth É, Blastyák A, Zhiponova M, Miskolczi P, Dudits D (2006) Activation of an alfalfa cyclin-dependent kinase inhibitor by calmodulin-like domain protein kinase. Plant J 46: 111–123[CrossRef][Web of Science][Medline] Putnam ML, Miller ML (2007) Rhodococcus fascians in herbaceous perennials. Plant Dis 91: 1064–1076[CrossRef] Riou-Khamlichi C, Huntley R, Jacqmard A, Murray JAH (1999) Cytokinin activation of Arabidopsis cell division through a D-type cyclin. Science 283: 1541–1544 Riou-Khamlichi C, Menges M, Healy JMS, Murray JAH (2000) Sugar control of the plant cell cycle: differential regulation of Arabidopsis D-type cyclin gene expression. Mol Cell Biol 20: 4513–4521 Schnittger A, Schöbinger U, Bouyer D, Weinl C, Stierhof Y-D, Hülskamp M (2002) Ectopic D-type cyclin expression induces not only DNA replication but also cell division in Arabidopsis trichomes. Proc Natl Acad Sci USA 99: 6410–6415 Schnittger A, Weinl C, Bouyer D, Schöbinger U, Hülskamp M (2003) Misexpression of the cyclin-dependent kinase inhibitor ICK1/KRP1 in single-celled Arabidopsis trichomes reduces endoreduplication and cell size and induces cell death. Plant Cell 15: 303–315 Simón-Mateo C, Depuydt S, de Oliveira Manes CL, Cnudde F, Holsters M, Goethals K, Vereecke D (2006) The phytopathogen Rhodococcus fascians breaks apical dominance and activates axillary meristems by inducing plant genes involved in hormone metabolism. Mol Plant Pathol 7: 103–112[CrossRef][Web of Science] Soni R, Carmichael JP, Shah ZH, Murray JAH (1995) A family of cyclin D homologs from plants differentially controlled by growth regulators and containing the conserved retinoblastoma protein interaction motif. Plant Cell 7: 85–103[Abstract] Sorrell DA, Combettes B, Chaubet-Gigot N, Gigot C, Murray JAH (1999) Distinct cyclin D genes show mitotic accumulation or constant levels of transcripts in tobacco Bright Yellow-2 cells. Plant Physiol 119: 343–351 Spíchal L, Kry Stals H, Inzé D (2001) When plant cells decide to divide. Trends Plant Sci 6: 359–364[CrossRef][Web of Science][Medline] Temmerman W, Vereecke D, Dreesen R, Van Montagu M, Holsters M, Goethals K (2000) Leafy gall formation is controlled by fasR, an AraC-type regulatory gene, in Rhodococcus fascians. J Bacteriol 182: 5832–5840 Traas J, Hülskamp M, Gendreau E, Höfte H (1998) Endoreduplication and development: rule without dividing? Curr Opin Plant Biol 1: 498–503[CrossRef][Web of Science][Medline] Tsukaya H (2006) Mechanism of leaf-shape determination. Annu Rev Plant Biol 57: 477–496[CrossRef][Medline] Vandeputte O, Öden S, Mol A, Vereecke D, Goethals K, El Jaziri M, Prinsen E (2005) Biosynthesis of auxin by the Gram-positive phytopathogen Rhodococcus fascians is controlled by compounds specific to infected plant tissues. Appl Environ Microbiol 71: 1169–1177 Vandeputte O, Vereecke D, Mol A, Lenjou M, Van Bockstaele D, El Jaziri M, Baucher M (2007) Rhodococcus fascians infection accelerates progression of tobacco BY-2 cells into mitosis through rapid changes in plant gene expression. New Phytol 175: 140–154[CrossRef][Web of Science][Medline] Vereecke D, Burssens S, Simón-Mateo C, Inzé D, Van Montagu M, Goethals K, Jaziri M (2000) The Rhodococcus fascians-plant interaction: morphological traits and biotechnological applications. Planta 210: 241–251[CrossRef][Web of Science][Medline] Vereecke D, Cornelis K, Temmerman W, Holsters M, Goethals K (2002a) Versatile persistence pathways for pathogens of animals and plants. Trends Microbiol 10: 485–488[CrossRef][Web of Science][Medline] Vereecke D, Cornelis K, Temmerman W, Jaziri M, Van Montagu M, Holsters M, Goethals K (2002b) Chromosomal locus that affects the pathogenicity of Rhodococcus fascians. J Bacteriol 184: 1112–1120 Verkest A, de O Manes C-L, Vercruysse S, Maes S, Van Der Schueren E, Beeckman T, Genschik P, Kuiper M, Inzé D, De Veylder L (2005) The cyclin-dependent kinase inhibitor KRP2 controls the onset of the endoreduplication cycle during Arabidopsis leaf development through inhibition of mitotic CDKA;1 kinase complexes. Plant Cell 17: 1723–1736 Vlieghe K, Boudolf V, Beemster GTS, Maes S, Magyar Z, Atanassova A, de Almeida Engler J, De Groodt R, Inzé D, De Veylder L (2005) The DP-E2F-like DEL1 gene controls the endocycle in Arabidopsis thaliana. Curr Biol 15: 59–63[CrossRef][Web of Science][Medline] Wang H, Qi Q, Schorr P, Cutler AJ, Crosby WL, Fowke LC (1998) ICK1, a cyclin-dependent protein kinase inhibitor from Arabidopsis thaliana interacts with both Cdc2a and CycD3, and its expression is induced by abscisic acid. Plant J 15: 501–510[CrossRef][Web of Science][Medline] Weinl C, Marquardt S, Kuijt SJH, Nowack MK, Jakoby MJ, Hülskamp M, Schnittger A (2005) Novel functions of plant cyclin-dependent kinase inhibitors, ICK1/KRP1, can act non-cell-autonomously and inhibit entry into mitosis. Plant Cell 17: 1704–1722 Zhang K, Diederich L, John PCI (2005) The cytokinin requirement for cell division in cultured Nicotiana plumbaginifolia cells can be satisfied by yeast Cdc25 protein tyrosine phosphatase: implications for mechanisms of cytokinin response and plant development. Plant Physiol 137: 308–316 Zhang Y, Wang Z, Ravid K (1996) The cell cycle in polyploid megakaryocytes is associated with reduced activity of cyclin B1-dependent Cdc2 kinase. J Biol Chem 271: 4266–4272 Related articles in Plant Physiol.:
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al K, Van Lijsebettens M, Moritz T, Holsters M, Vereecke D (2008) Modulation of the hormone setting by Rhodococcus fascians results in ectopic KNOX activation in Arabidopsis. Plant Physiol 146: 1267–1281
tof V, PaprskáŸová Lenobel R, St
skala J, Binarová P, Cenklová V, De Veylder L, Inzé D, Kontopidis G, Fischer PM, et al (2007) Classical anticytokinins do not interact with cytokinin receptors but inhibit cyclin-dependent kinases. J Biol Chem 282: 14356–14363
