Research
In many dicot plants lateral roots arise from a dedicated cell file of the main root called pericycle. Initiation of lateral roots requires the phytohormone auxin that first triggers critical asymmetric cell divisions in the pericycle then acts as an instructive signal for lateral root growth and development.
While recent works have provided a large body of information concerning the role of auxin signaling and identified elements of the signaling pathway, our knowledge of the mechanism acting downstream of the auxin signal is still limited. In particular, we have just begun to understand the mechanism controlling the first critical formative pericycle divisions.
Plant growth depends on a root system that anchors plant in the soil and functions as an entry site for water and essential nutrients. Development of the root system is a post-embryonic process during which a highly branched network of lateral roots forms.
We have been studying lateral root initiation in the model plant Arabidopsis thaliana and identified a novel molecular mechanism that appears to regulate asymmetric pericycle cell divisions. Main components of this mechanism are the RETINOBLASTOMA-RELATED PROTEIN1 (RBR1) and the ATP-dependent chromatin remodeler PICKLE (PKL) that associates with RBR1. The RBR1-PKL complex negatively regulates expression of certain LDB genes whose activity is required for asymmetric pericycle cell division and lateral root initiation.
We are using biochemical, genetic and cell biology methods to elaborate on this repressor function and better understand the molecular mechanism which directs the RBR1-PKL complex to target loci, to dissect the subunit structure of the holocomplex and to elucidate how auxin signaling dissociate the complex. In ChIP-seq experiments we address the question whether the RBR1-PKL complex plays roles in other plant developmental processes.
Key Publications
- Cruz-Ramírez A, Díaz-Triviño S, Blilou I, Grieneisen VA, Sozzani R, Zamioudis C, Miskolczi P, Nieuwland J, Benjamins R, Dohnuk- se P, Caballero-Pérez J, Horvath B, Long Y, Mähonën AP, Xu J, Murray JA, Benfey PN, Bakó L, Marée AF, Scheres B, (2012). A bis-table circuit involving SCARECROW-RETINOBLASTOMA integrates cues to inform asymmetric stem cell division. Cell 150:1002-15.
- Magyar Z, Horváth B, Khan S, Mohammed B, Henriques R, De Veylder L, Bakó L, Scheres B, Bögre L (2012). Arabidopsis E2FA stimulates proliferation and endocycle separately through RBR-bound and RBR-free complexes. EMBO J. 31:1480-1493.
- Karlberg A, Bakó L, Bhalerao RP. (2011). Short day-mediated cessation of growth requires the downregulation of AINTEGUMENTALI- KE1 transcription factor in hybrid aspen. PLoS Genet. 7(11):e1002361.
- Ábrahám E, Miskolczi P, Ayaydin F, Yu P, Kotogány E, Bakó L, Ötvös K, Horváth GV, Dudits D. (2011). Immunodetection of retino- blastoma-related protein and its phosphorylated form in interphase and mitotic alfalfa cells. J Exp Bot. 62:2155-2168.
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Publications
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Paper link bibtex abstract
@article{jurca_zeitlupe_2022, title = {{ZEITLUPE} {Promotes} {ABA}-{Induced} {Stomatal} {Closure} in {Arabidopsis} and {Populus}}, volume = {13}, issn = {1664-462X}, url = {https://www.frontiersin.org/article/10.3389/fpls.2022.829121}, abstract = {Plants balance water availability with gas exchange and photosynthesis by controlling stomatal aperture. This control is regulated in part by the circadian clock, but it remains unclear how signalling pathways of daily rhythms are integrated into stress responses. The serine/threonine protein kinase OPEN STOMATA 1 (OST1) contributes to the regulation of stomatal closure via activation of S-type anion channels. OST1 also mediates gene regulation in response to ABA/drought stress. We show that ZEITLUPE (ZTL), a blue light photoreceptor and clock component, also regulates ABA-induced stomatal closure in Arabidopsis thaliana, establishing a link between clock and ABA-signalling pathways. ZTL sustains expression of OST1 and ABA-signalling genes. Stomatal closure in response to ABA is reduced in ztl mutants, which maintain wider stomatal apertures and show higher rates of gas exchange and water loss than wild-type plants. Detached rosette leaf assays revealed a stronger water loss phenotype in ztl-3, ost1-3 double mutants, indicating that ZTL and OST1 contributed synergistically to the control of stomatal aperture. Experimental studies of Populus sp., revealed that ZTL regulated the circadian clock and stomata, indicating ZTL function was similar in these trees and Arabidopsis. PSEUDO-RESPONSE REGULATOR 5 (PRR5), a known target of ZTL, affects ABA-induced responses, including stomatal regulation. Like ZTL, PRR5 interacted physically with OST1 and contributed to the integration of ABA responses with circadian clock signalling. This suggests a novel mechanism whereby the PRR proteins—which are expressed from dawn to dusk—interact with OST1 to mediate ABA-dependent plant responses to reduce water loss in time of stress.}, urldate = {2022-03-02}, journal = {Frontiers in Plant Science}, author = {Jurca, Manuela and Sjölander, Johan and Ibáñez, Cristian and Matrosova, Anastasia and Johansson, Mikael and Kozarewa, Iwanka and Takata, Naoki and Bakó, Laszlo and Webb, Alex A. R. and Israelsson-Nordström, Maria and Eriksson, Maria E.}, month = mar, year = {2022}, keywords = {⛔ No DOI found}, }
Paper doi link bibtex abstract 8 downloads
@article{otvos_pickle_2021, title = {Pickle {Recruits} {Retinoblastoma} {Related} 1 to {Control} {Lateral} {Root} {Formation} in {Arabidopsis}}, volume = {22}, copyright = {http://creativecommons.org/licenses/by/3.0/}, url = {https://www.mdpi.com/1422-0067/22/8/3862}, doi = {10.3390/ijms22083862}, abstract = {Lateral root (LR) formation is an example of a plant post-embryonic organogenesis event. LRs are issued from non-dividing cells entering consecutive steps of formative divisions, proliferation and elongation. The chromatin remodeling protein PICKLE (PKL) negatively regulates auxin-mediated LR formation through a mechanism that is not yet known. Here we show that PKL interacts with RETINOBLASTOMA-RELATED 1 (RBR1) to repress the LATERAL ORGAN BOUNDARIES-DOMAIN 16 (LBD16) promoter activity. Since LBD16 function is required for the formative division of LR founder cells, repression mediated by the PKL–RBR1 complex negatively regulates formative division and LR formation. Inhibition of LR formation by PKL–RBR1 is counteracted by auxin, indicating that, in addition to auxin-mediated transcriptional responses, the fine-tuned process of LR formation is also controlled at the chromatin level in an auxin-signaling dependent manner.}, language = {en}, number = {8}, urldate = {2021-07-01}, journal = {International Journal of Molecular Sciences}, author = {Ötvös, Krisztina and Miskolczi, Pál and Marhavý, Peter and Cruz-Ramírez, Alfredo and Benková, Eva and Robert, Stéphanie and Bakó, László}, month = jan, year = {2021}, keywords = {\textit{de novo} organogenesis, auxin signaling, chromatin remodeling}, pages = {3862}, }
Paper doi link bibtex
@article{espinal-centeno_conservation_2020, title = {Conservation analysis of core cell cycle regulators and their transcriptional behavior during limb regeneration in {Ambystoma} mexicanum}, volume = {164}, issn = {09254773}, url = {https://linkinghub.elsevier.com/retrieve/pii/S0925477320300563}, doi = {10.1016/j.mod.2020.103651}, language = {en}, urldate = {2021-06-07}, journal = {Mechanisms of Development}, author = {Espinal-Centeno, Annie and Dipp-Álvarez, Melissa and Saldaña, Carlos and Bakó, Laszlo and Cruz-Ramírez, Alfredo}, month = dec, year = {2020}, pages = {103651}, }
Paper doi link bibtex abstract 5 downloads
@article{zhang_chromatin-modifying_2020, title = {The chromatin-modifying protein {HUB2} is involved in the regulation of lignin composition in xylem vessels}, volume = {71}, issn = {0022-0957, 1460-2431}, url = {https://academic.oup.com/jxb/article/71/18/5484/5849544}, doi = {10.1093/jxb/eraa264}, abstract = {Abstract PIRIN2 (PRN2) was earlier reported to suppress syringyl (S)-type lignin accumulation of xylem vessels of Arabidopsis thaliana. In the present study, we report yeast two-hybrid results supporting the interaction of PRN2 with HISTONE MONOUBIQUITINATION2 (HUB2) in Arabidopsis. HUB2 has been previously implicated in several plant developmental processes, but not in lignification. Interaction between PRN2 and HUB2 was verified by β-galactosidase enzymatic and co-immunoprecipitation assays. HUB2 promoted the deposition of S-type lignin in the secondary cell walls of both stem and hypocotyl tissues, as analysed by pyrolysis-GC/MS. Chemical fingerprinting of individual xylem vessel cell walls by Raman and Fourier transform infrared microspectroscopy supported the function of HUB2 in lignin deposition. These results, together with a genetic analysis of the hub2 prn2 double mutant, support the antagonistic function of PRN2 and HUB2 in deposition of S-type lignin. Transcriptome analyses indicated the opposite regulation of the S-type lignin biosynthetic gene FERULATE-5-HYDROXYLASE1 by PRN2 and HUB2 as the underlying mechanism. PRN2 and HUB2 promoter activities co-localized in cells neighbouring the xylem vessel elements, suggesting that the S-type lignin-promoting function of HUB2 is antagonized by PRN2 for the benefit of the guaiacyl (G)-type lignin enrichment of the neighbouring xylem vessel elements.}, language = {en}, number = {18}, urldate = {2021-06-07}, journal = {Journal of Experimental Botany}, author = {Zhang, Bo and Sztojka, Bernadette and Seyfferth, Carolin and Escamez, Sacha and Miskolczi, Pál and Chantreau, Maxime and Bakó, László and Delhomme, Nicolas and Gorzsás, András and Bhalerao, Rishikesh P. and Tuominen, Hannele}, editor = {Turner, Simon}, month = sep, year = {2020}, pages = {5484--5494}, }
Paper doi link bibtex
@article{lakehal_molecular_2019, title = {A {Molecular} {Framework} for the {Control} of {Adventitious} {Rooting} by {TIR1}/{AFB2}-{Aux}/{IAA}-{Dependent} {Auxin} {Signaling} in {Arabidopsis}}, volume = {12}, issn = {16742052}, url = {https://linkinghub.elsevier.com/retrieve/pii/S1674205219302904}, doi = {10.1016/j.molp.2019.09.001}, language = {en}, number = {11}, urldate = {2021-06-07}, journal = {Molecular Plant}, author = {Lakehal, Abdellah and Chaabouni, Salma and Cavel, Emilie and Le Hir, Rozenn and Ranjan, Alok and Raneshan, Zahra and Novák, Ondřej and Păcurar, Daniel I. and Perrone, Irene and Jobert, François and Gutierrez, Laurent and Bakó, Laszlo and Bellini, Catherine}, month = nov, year = {2019}, pages = {1499--1514}, }
Paper doi link bibtex 1 download
@article{chahtane_leafy_2018, title = {{LEAFY} activity is post-transcriptionally regulated by {BLADE} {ON} {PETIOLE2} and {CULLIN3} in {Arabidopsis}}, volume = {220}, issn = {0028646X}, url = {http://doi.wiley.com/10.1111/nph.15329}, doi = {10/gfcdwc}, language = {en}, number = {2}, urldate = {2021-06-07}, journal = {New Phytologist}, author = {Chahtane, Hicham and Zhang, Bo and Norberg, Mikael and LeMasson, Marie and Thévenon, Emmanuel and Bakó, László and Benlloch, Reyes and Holmlund, Mattias and Parcy, François and Nilsson, Ove and Vachon, Gilles}, month = oct, year = {2018}, pages = {579--592}, }
Paper doi link bibtex
@article{caballero-perez_transcriptional_2018, title = {Transcriptional landscapes of {Axolotl} ({Ambystoma} mexicanum)}, volume = {433}, issn = {00121606}, url = {https://linkinghub.elsevier.com/retrieve/pii/S0012160617302786}, doi = {10/gcwm2z}, language = {en}, number = {2}, urldate = {2021-06-07}, journal = {Developmental Biology}, author = {Caballero-Pérez, Juan and Espinal-Centeno, Annie and Falcon, Francisco and García-Ortega, Luis F. and Curiel-Quesada, Everardo and Cruz-Hernández, Andrés and Bakó, Laszlo and Chen, Xuemei and Martínez, Octavio and Alberto Arteaga-Vázquez, Mario and Herrera-Estrella, Luis and Cruz-Ramírez, Alfredo}, month = jan, year = {2018}, pages = {227--239}, }
Paper doi link bibtex abstract
@article{zhang_blade--petiole_2017, title = {{BLADE}-{ON}-{PETIOLE} proteins act in an {E3} ubiquitin ligase complex to regulate {PHYTOCHROME} {INTERACTING} {FACTOR} 4 abundance}, volume = {6}, issn = {2050-084X}, url = {https://elifesciences.org/articles/26759}, doi = {10/gb2fm5}, abstract = {Both light and temperature have dramatic effects on plant development. Phytochrome photoreceptors regulate plant responses to the environment in large part by controlling the abundance of PHYTOCHROME INTERACTING FACTOR (PIF) transcription factors. However, the molecular determinants of this essential signaling mechanism still remain largely unknown. Here, we present evidence that the BLADE-ON-PETIOLE (BOP) genes, which have previously been shown to control leaf and flower development in Arabidopsis, are involved in controlling the abundance of PIF4. Genetic analysis shows that BOP2 promotes photo-morphogenesis and modulates thermomorphogenesis by suppressing PIF4 activity, through a reduction in PIF4 protein level. In red-light-grown seedlings PIF4 ubiquitination was reduced in the bop2 mutant. Moreover, we found that BOP proteins physically interact with both PIF4 and CULLIN3A and that a CULLIN3-BOP2 complex ubiquitinates PIF4 in vitro. This shows that BOP proteins act as substrate adaptors in a CUL3BOP1/BOP2 E3 ubiquitin ligase complex, targeting PIF4 proteins for ubiquitination and subsequent degradation.}, language = {en}, urldate = {2021-06-07}, journal = {eLife}, author = {Zhang, Bo and Holmlund, Mattias and Lorrain, Severine and Norberg, Mikael and Bakó, László and Fankhauser, Christian and Nilsson, Ove}, month = aug, year = {2017}, pages = {e26759}, }
Paper doi link bibtex
@article{zhao_xylem_2017, title = {{XYLEM} {NAC} {DOMAIN1}, an angiosperm {NAC} transcription factor, inhibits xylem differentiation through conserved motifs that interact with {RETINOBLASTOMA}‐{RELATED}}, volume = {216}, issn = {0028-646X, 1469-8137}, url = {https://onlinelibrary.wiley.com/doi/10.1111/nph.14704}, doi = {10/gbt5ht}, language = {en}, number = {1}, urldate = {2021-06-07}, journal = {New Phytologist}, author = {Zhao, Chengsong and Lasses, Theres and Bakó, Laszlo and Kong, Danyu and Zhao, Bingyu and Chanda, Bidisha and Bombarely, Aureliano and Cruz‐Ramírez, Alfredo and Scheres, Ben and Brunner, Amy M. and Beers, Eric P.}, month = oct, year = {2017}, pages = {76--89}, }
Paper doi link bibtex
@article{cruz-santos_role_2016, title = {The {Role} of {microRNAs} in {Animal} {Cell} {Reprogramming}}, volume = {25}, issn = {1547-3287, 1557-8534}, url = {https://www.liebertpub.com/doi/10.1089/scd.2015.0359}, doi = {10/f3rw7p}, language = {en}, number = {14}, urldate = {2021-06-07}, journal = {Stem Cells and Development}, author = {Cruz-Santos, María Concepción and Aragón-Raygoza, Alejandro and Espinal-Centeno, Annie and Arteaga-Vázquez, Mario and Cruz-Hernández, Andrés and Bakó, Laszlo and Cruz-Ramírez, Alfredo}, month = jul, year = {2016}, pages = {1035--1049}, }
Paper doi link bibtex
@article{le_hir_abcg9_2013, title = {{ABCG9}, {ABCG11} and {ABCG14} {ABC} transporters are required for vascular development in {Arabidopsis}}, volume = {76}, issn = {09607412}, url = {http://doi.wiley.com/10.1111/tpj.12334}, doi = {10/f22xd4}, language = {en}, number = {5}, urldate = {2021-06-08}, journal = {The Plant Journal}, author = {Le Hir, Rozenn and Sorin, Clément and Chakraborti, Dipankar and Moritz, Thomas and Schaller, Hubert and Tellier, Frédérique and Robert, Stéphanie and Morin, Halima and Bakó, Laszlo and Bellini, Catherine}, month = dec, year = {2013}, pages = {811--824}, }
Paper doi link bibtex
@article{cruz-ramirez_bistable_2012, title = {A {Bistable} {Circuit} {Involving} {SCARECROW}-{RETINOBLASTOMA} {Integrates} {Cues} to {Inform} {Asymmetric} {Stem} {Cell} {Division}}, volume = {150}, issn = {00928674}, url = {https://linkinghub.elsevier.com/retrieve/pii/S009286741200880X}, doi = {10/f3n3f8}, language = {en}, number = {5}, urldate = {2021-06-08}, journal = {Cell}, author = {Cruz-Ramírez, Alfredo and Díaz-Triviño, Sara and Blilou, Ikram and Grieneisen, Verônica A. and Sozzani, Rosangela and Zamioudis, Christos and Miskolczi, Pál and Nieuwland, Jeroen and Benjamins, René and Dhonukshe, Pankaj and Caballero-Pérez, Juan and Horvath, Beatrix and Long, Yuchen and Mähönen, Ari Pekka and Zhang, Hongtao and Xu, Jian and Murray, James A.H. and Benfey, Philip N. and Bakó, Laszlo and Marée, Athanasius F.M. and Scheres, Ben}, month = aug, year = {2012}, pages = {1002--1015}, }
Paper doi link bibtex abstract
@article{magyar_arabidopsis_2012, title = {Arabidopsis {E2FA} stimulates proliferation and endocycle separately through {RBR}-bound and {RBR}-free complexes}, volume = {31}, issn = {0261-4189}, url = {https://www.embopress.org/doi/full/10.1038/emboj.2012.13}, doi = {10/f24b6f}, abstract = {Post-embryonic growth in plants depends on the continuous supply of undifferentiated cells within meristems. Proliferating cells maintain their competence for division by active repression of differentiation and the associated endocycle entry. We show by upregulation and downregulation of E2FA that it is required for maintaining proliferation, as well as for endocycle entry. While E2FB?RBR1 (retinoblastoma-related protein 1) complexes are reduced after sucrose addition or at elevated CYCD3;1 levels, E2FA maintains a stable complex with RBR1 in proliferating cells. Chromatin immunoprecipitation shows that RBR1 binds in the proximity of E2F promoter elements in CCS52A1 and CSS52A2 genes, central regulators for the switch from proliferation to endocycles. Overexpression of a truncated E2FA mutant (E2FA?RB) lacking the RBR1-binding domain interferes with RBR1 recruitment to promoters through E2FA, leading to decreased meristem size in roots, premature cell expansion and hyperactivated endocycle in leaves. E2F target genes, including CCS52A1 and CCS52A2, are upregulated in E2FA?RB and e2fa knockout lines. These data suggest that E2FA in complex with RBR1 forms a repressor complex in proliferating cells to inhibit premature differentiation and endocycle entry. Thus, E2FA regulates organ growth via two distinct, sequentially operating pathways.}, number = {6}, urldate = {2021-06-21}, journal = {The EMBO Journal}, author = {Magyar, Zoltán and Horváth, Beatrix and Khan, Safina and Mohammed, Binish and Henriques, Rossana and De Veylder, Lieven and Bakó, László and Scheres, Ben and Bögre, László}, month = mar, year = {2012}, note = {Publisher: John Wiley \& Sons, Ltd}, keywords = {Arabidopsis, E2F, cell proliferation, endocycle, retinoblastoma}, pages = {1480--1493}, }
Paper doi link bibtex 2 downloads
@article{shaikhali_cryptochrome1-dependent_2012, title = {The {CRYPTOCHROME1}-{Dependent} {Response} to {Excess} {Light} {Is} {Mediated} through the {Transcriptional} {Activators} {ZINC} {FINGER} {PROTEIN} {EXPRESSED} {IN} {INFLORESCENCE} {MERISTEM} {LIKE1} and {ZML2} in {Arabidopsis}}, volume = {24}, issn = {1040-4651, 1532-298X}, url = {https://academic.oup.com/plcell/article/24/7/3009-3025/6100855}, doi = {10/f23c7q}, language = {en}, number = {7}, urldate = {2021-06-08}, journal = {The Plant Cell}, author = {Shaikhali, Jehad and de Dios Barajas-Lopéz, Juan and Ötvös, Krisztina and Kremnev, Dmitry and Garcia, Ana Sánchez and Srivastava, Vaibhav and Wingsle, Gunnar and Bakó, Laszlo and Strand, Åsa}, month = jul, year = {2012}, pages = {3009--3025}, }
Paper doi link bibtex
@article{buren_use_2012, title = {Use of the {Foot}-and-{Mouth} {Disease} {Virus} {2A} {Peptide} {Co}-{Expression} {System} to {Study} {Intracellular} {Protein} {Trafficking} in {Arabidopsis}}, volume = {7}, issn = {1932-6203}, url = {https://dx.plos.org/10.1371/journal.pone.0051973}, doi = {10/f224q9}, language = {en}, number = {12}, urldate = {2021-06-08}, journal = {PLoS ONE}, author = {Burén, Stefan and Ortega-Villasante, Cristina and Ötvös, Krisztina and Samuelsson, Göran and Bakó, László and Villarejo, Arsenio}, editor = {Caplan, Steve}, month = dec, year = {2012}, pages = {e51973}, }
Paper doi link bibtex
@article{baba_activity-dormancy_2011, title = {Activity-dormancy transition in the cambial meristem involves stage-specific modulation of auxin response in hybrid aspen}, volume = {108}, issn = {0027-8424, 1091-6490}, url = {http://www.pnas.org/cgi/doi/10.1073/pnas.1011506108}, doi = {10/d34mx2}, language = {en}, number = {8}, urldate = {2021-06-08}, journal = {Proceedings of the National Academy of Sciences}, author = {Baba, K. and Karlberg, A. and Schmidt, J. and Schrader, J. and Hvidsten, T. R. and Bakó, L. and Bhalerao, Rishikesh P.}, month = feb, year = {2011}, pages = {3418--3423}, }
Paper doi link bibtex
@article{abraham_immunodetection_2011, title = {Immunodetection of retinoblastoma-related protein and its phosphorylated form in interphase and mitotic alfalfa cells}, volume = {62}, issn = {0022-0957, 1460-2431}, url = {https://academic.oup.com/jxb/article-lookup/doi/10.1093/jxb/erq413}, doi = {10/dz5rcb}, language = {en}, number = {6}, urldate = {2021-06-08}, journal = {Journal of Experimental Botany}, author = {Abraham, E. and Miskolczi, P. and Ayaydin, F. and Yu, P. and Kotogany, E. and Bakó, L. and Otvos, K. and Horvath, G. V. and Dudits, D.}, month = mar, year = {2011}, pages = {2155--2168}, }
Paper doi link bibtex
@article{buren_importance_2011, title = {Importance of {Post}-{Translational} {Modifications} for {Functionality} of a {Chloroplast}-{Localized} {Carbonic} {Anhydrase} ({CAH1}) in {Arabidopsis} thaliana}, volume = {6}, issn = {1932-6203}, url = {https://dx.plos.org/10.1371/journal.pone.0021021}, doi = {10/bdgdgk}, language = {en}, number = {6}, urldate = {2021-06-08}, journal = {PLoS ONE}, author = {Burén, Stefan and Ortega-Villasante, Cristina and Blanco-Rivero, Amaya and Martínez-Bernardini, Andrea and Shutova, Tatiana and Shevela, Dmitriy and Messinger, Johannes and Bakó, Laszlo and Villarejo, Arsenio and Samuelsson, Göran}, editor = {Bassham, Diane}, month = jun, year = {2011}, pages = {e21021}, }
Paper doi link bibtex abstract 1 download
@article{johansson_partners_2011, title = {Partners in {Time}: {EARLY} {BIRD} {Associates} with {ZEITLUPE} and {Regulates} the {Speed} of the {Arabidopsis} {Clock}}, volume = {155}, issn = {1532-2548}, shorttitle = {Partners in {Time}}, url = {https://academic.oup.com/plphys/article/155/4/2108/6108867}, doi = {10/bgh2rc}, abstract = {Abstract The circadian clock of the model plant Arabidopsis (Arabidopsis thaliana) is made up of a complex series of interacting feedback loops whereby proteins regulate their own expression across day and night. early bird (ebi) is a circadian mutation that causes the clock to speed up: ebi plants have short circadian periods, early phase of clock gene expression, and are early flowering. We show that EBI associates with ZEITLUPE (ZTL), known to act in the plant clock as a posttranslational mediator of protein degradation. However, EBI is not degraded by its interaction with ZTL. Instead, ZTL counteracts the effect of EBI during the day and increases it at night, modulating the expression of key circadian components. The partnership of EBI with ZTL reveals a novel mechanism involved in controlling the complex transcription-translation feedback loops of the clock. This work highlights the importance of cross talk between the ubiquitination pathway and transcriptional control for regulation of the plant clock.}, language = {en}, number = {4}, urldate = {2021-06-08}, journal = {Plant Physiology}, author = {Johansson, Mikael and McWatters, Harriet G. and Bakó, László and Takata, Naoki and Gyula, Péter and Hall, Anthony and Somers, David E. and Millar, Andrew J. and Eriksson, Maria E.}, month = mar, year = {2011}, pages = {2108--2122}, }
Paper doi link bibtex
@article{karlberg_short_2011, title = {Short {Day}–{Mediated} {Cessation} of {Growth} {Requires} the {Downregulation} of {AINTEGUMENTALIKE1} {Transcription} {Factor} in {Hybrid} {Aspen}}, volume = {7}, issn = {1553-7404}, url = {https://dx.plos.org/10.1371/journal.pgen.1002361}, doi = {10/dx44wg}, language = {en}, number = {11}, urldate = {2021-06-08}, journal = {PLoS Genetics}, author = {Karlberg, Anna and Bakó, Laszlo and Bhalerao, Rishikesh P.}, editor = {Sederoff, Ronald R.}, month = nov, year = {2011}, pages = {e1002361}, }
doi link bibtex abstract 2 downloads
@article{karlberg_analysis_2010, title = {Analysis of global changes in gene expression during activity-dormancy cycle in hybrid aspen apex}, volume = {27}, doi = {10/frkc7v}, abstract = {Perennial plants such as the long-lived trees of boreal forest cycle between periods of active growth and dormancy. Transition from active growth to dormancy is induced by short day (SD) signal. Once dormancy is established, prolonged exposure to low temperature is required for breaking dormancy before warm temperatures can induce growth. We have studied global changes in gene expression in the apex of model plant hybrid aspen during the distinct stages of activity-dormancy cycle. Our data shows that all stages of activity-dormancy cycle in the apex are associated with substantial modulation of the transcriptome. Detailed analysis of core cell cycle genes indicates that with the exception of plant specific B-type CDKs, all of the other CDKs are regulated post-transcriptionally during growth cessation. SD signal appears to target the expression of cyclin genes that are down regulated during growth arrest. Several of the cold hardiness related genes e. g. dehydrins are induced during transition to dormancy although temperature is not reduced and the up-regulation of the expression of these genes does not appear to rely on SD mediated induction of classical CBF transcription factors. Our results suggest that transcriptional control plays a key role in modulation of hormones such as ABA and GA that are known to play a central role in various processes during activity-dormancy cycle. Analysis of histone and DNA modification genes indicates that chromatin remodeling could be involved in coordinating global changes in gene expression during activity-dormancy cycle.}, number = {1}, journal = {Plant Biotechnology}, author = {Karlberg, Anna and Englund, Madeleine and Petterle, Anna and Molnar, Gergely and Sjödin, Andreas and Bakó, Laszlo and Bhalerao, Rishikesh P.}, year = {2010}, keywords = {Cell cycle, dormancy, hormone, microarray, poplar}, pages = {1--16}, }
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@article{pettko-szandtner_activation_2006, title = {Activation of an alfalfa cyclin-dependent kinase inhibitor by calmodulin-like domain protein kinase}, volume = {46}, issn = {0960-7412}, doi = {10/b4vt9r}, abstract = {Kip- related proteins ( KRPs) play a central role in the regulation of the cell cycle and differentiation through modulation of cyclin- dependent kinase ( CDK) functions. We have identified a CDK inhibitor gene from Medicago truncatula ( Mt) by a yeast two- hybrid screen. The KRPMt gene was expressed in all plant organs and cultured cells, and its transcripts accumulated after abscisic acid and NaCl treatment. The KRPMt protein exhibits seven conserved sequence domains and a PEST motif that is also detected in various Arabidopsis KRPs. In the yeast two- hybrid test, the KRPMt protein interacted with CDK ( Medsa; CDKA; 1) and D- type cyclins. However, in the pull- down assays, B- type CDK complexes were also detectable. Recombinant KRPMt differentially inhibited various alfalfa CDK complexes in phosphorylation assays. The immunoprecipitated Medsa; CDKA; 1/ A; 2 complex was strongly inhibited, whereas the mitotic Medsa; CDKB2; 1 complex was the most sensitive to inhibition. Function of Medsa; CDKB1; 1 complex was not inhibited by the KRPMt protein. The mitotic Medsa; CYCB2 and Medsa; CYCA2; 1 complexes responded weakly to this inhibitor protein. Kinase complexes from G2/ M cells showed increased sensitivity towards the inhibitor compared with those isolated from G1/ S- phase cells. In vitro phosphorylation of Medicago retinoblastoma- related protein was also reduced in the presence of KRPMt. Phosphorylation of this inhibitor protein by the recombinant calmodulin- like domain protein kinase ( MsCPK3) resulted in enhanced inhibition of CDK function. The data presented emphasize the selective sensitivity of various cyclin- dependent kinase complexes to this inhibitor protein, and suggest a role for CDK inhibitors and CPKs in cross- talk between Ca2+ signalling and regulation of cell- cycle progression in plants.}, language = {English}, number = {1}, journal = {Plant Journal}, author = {Pettko-Szandtner, A. and Meszaros, T. and Horvath, G. V. and Bakó, L. and Csordas-Toth, E. and Blastyak, A. and Zhiponova, M. and Miskolczi, P. and Dudits, D.}, month = apr, year = {2006}, note = {Place: Hoboken Publisher: Wiley WOS:000236035700008}, keywords = {Ca2+ signalling, abscisic acid, arabidopsis-thaliana, calcium, cell cycle, cyclin-dependent kinase, expression, gene family, ick1, in-vitro, medicago-sativa, phosphorylation, plant-cell cycle, retinoblastoma-related protein}, pages = {111--123}, }
Paper doi link bibtex abstract
@article{horvath_ebp1_2006, title = {{EBP1} regulates organ size through cell growth and proliferation in plants}, volume = {25}, issn = {0261-4189}, url = {https://www.embopress.org/doi/full/10.1038/sj.emboj.7601362}, doi = {10.1038/sj.emboj.7601362}, abstract = {Plant organ size shows remarkable uniformity within species indicating strong endogenous control. We have identified a plant growth regulatory gene, functionally and structurally homologous to human EBP1. Plant EBP1 levels are tightly regulated; gene expression is highest in developing organs and correlates with genes involved in ribosome biogenesis and function. EBP1 protein is stabilised by auxin. Elevating or decreasing EBP1 levels in transgenic plants results in a dose-dependent increase or reduction in organ growth, respectively. During early stages of organ development, EBP1 promotes cell proliferation, influences cell-size threshold for division and shortens the period of meristematic activity. In postmitotic cells, it enhances cell expansion. EBP1 is required for expression of cell cycle genes; CyclinD3;1, ribonucleotide reductase 2 and the cyclin-dependent kinase B1;1. The regulation of these genes by EBP1 is dose and auxin dependent and might rely on the effect of EBP1 to reduce RBR1 protein level. We argue that EBP1 is a conserved, dose-dependent regulator of cell growth that is connected to meristematic competence and cell proliferation via regulation of RBR1 level.}, number = {20}, urldate = {2021-06-11}, journal = {The EMBO Journal}, author = {Horváth, Beatrix M and Magyar, Zoltán and Zhang, Yuexing and Hamburger, Anne W and Bakó, László and Visser, Richard GF and Bachem, Christian WB and Bögre, László}, month = oct, year = {2006}, note = {Publisher: John Wiley \& Sons, Ltd}, keywords = {EBP1, arabidopsis, cell growth, cell proliferation, cycle regulation, differential gene-expression, division, ebp1, erbb-3 binding-protein, expansion, leaf, organ growth, organogenesis, potato-tuber development, ribosome biogenesis, transcription factor}, pages = {4909--4920}, }
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@article{fulop_arabidopsis_2005, title = {Arabidopsis {Anaphase}-{Promoting} {Complexes}: {Multiple} {Activators} and {Wide} {Range} of {Substrates} {Might} {Keep} {APC} {Perpetually} {Busy}}, volume = {4}, issn = {1538-4101}, shorttitle = {Arabidopsis {Anaphase}-{Promoting} {Complexes}}, url = {https://doi.org/10.4161/cc.4.8.1856}, doi = {10.4161/cc.4.8.1856}, abstract = {The anaphase-promoting complex (APC), a multisubunit E3 ubiquitin ligase, is anessential regulator of the cell cycle from metaphase until S phase in yeast and metazoans.APC mediates degradation of numerous cell cycle-related proteins, including mitoticcyclins and its activation and substrate-specificity are determined by two adaptor proteins,Cdc20 and Cdh1. Plants have multiple APC activators and the Cdh1-type proteins, inaddition, are represented by two subclasses, known as Ccs52A and Ccs52B. TheArabidopsis genome contains five cdc20 genes as well as ccs52A1, ccs52A2 and ccs52B. InSchizosaccharomyces pombe, expression of the three Atccs52 genes elicited distinctphenotypes supporting non-redundant function of the AtCcs52 proteins. Consistent withthese activities, the AtCcs52 proteins were able to bind both to the yeast and theArabidopsis APCs. In synchronized Arabidopsis cell cultures the cdc20 transcripts werepresent from early G2 until the M-phase exit, ccs52B from G2/M to M while ccs52A1 andccs52A2 were from late M until early G2, suggesting consecutive action of these APCactivators in the plant cell cycle. The AtCcs52 proteins interacted with different subsets ofmitotic cyclins, in accordance with their expression profiles, either in free- or CDK-boundforms. Expression of most APC subunits was constitutive, whereas cdc27a and cdc27b,corresponding to two forms of apc3, and ubc19 and ubc20 encoding E2-C type ubiquitinconjugatingenzymes displayed differences in their cell cycle regulation. These dataindicate the existence of numerous APCCdc20/Ccs52/Cdc27 forms in Arabidopsis, which inconjunction with different E2 enzymes might have distinct or complementary functions atdistinct stages of the cell cycle.}, number = {8}, urldate = {2021-10-14}, journal = {Cell Cycle}, author = {Fülöp, Katalin and Tarayre, Sylvie and Kelemen, Zsolt and Horváth, Gábor and Kevei, Zoltán and Nikovics, Krisztina and Bakó, László and Brown, Spencer and Kondorosi, Adam and Kondorosi, Eva}, month = aug, year = {2005}, pages = {4084--4092}, }
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@article{villarejo_evidence_2005, title = {Evidence for a protein transported through the secretory pathway en route to the higher plant chloroplast}, volume = {7}, copyright = {2005 Nature Publishing Group}, issn = {1476-4679}, url = {https://www.nature.com/articles/ncb1330}, doi = {10/fmrqwn}, abstract = {In contrast to animal and fungal cells, green plant cells contain one or multiple chloroplasts, the organelle(s) in which photosynthetic reactions take place. Chloroplasts are believed to have originated from an endosymbiotic event and contain DNA that codes for some of their proteins. Most chloroplast proteins are encoded by the nuclear genome and imported with the help of sorting signals that are intrinsic parts of the polypeptides. Here, we show that a chloroplast-located protein in higher plants takes an alternative route through the secretory pathway, and becomes N-glycosylated before entering the chloroplast.}, language = {en}, number = {12}, urldate = {2021-06-11}, journal = {Nature Cell Biology}, author = {Villarejo, Arsenio and Burén, Stefan and Larsson, Susanne and Déjardin, Annabelle and Monné, Magnus and Rudhe, Charlotta and Karlsson, Jan and Jansson, Stefan and Lerouge, Patrice and Rolland, Norbert and von Heijne, Gunnar and Grebe, Markus and Bakó, Laszlo and Samuelsson, Göran}, month = dec, year = {2005}, note = {Number: 12 Publisher: Nature Publishing Group}, pages = {1224--1231}, }
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@article{fulop_medicago_2005, title = {The {Medicago} {CDKC};1-{CYCLINT};1 kinase complex phosphorylates the carboxy-terminal domain of {RNA} polymerase {II} and promotes transcription}, volume = {42}, issn = {1365-313X}, url = {https://onlinelibrary.wiley.com/doi/abs/10.1111/j.1365-313X.2005.02421.x}, doi = {10/fmbqpx}, abstract = {The Ms;CDKC;1 kinase is structurally similar to those cyclin-dependent kinases (CDKs) that are not involved directly in cell cycle regulation. The presence of a PITAIRE motif in Ms;CDKC;1 suggests that it interacts with cyclins different from known PSTAIRE/PPTALRE kinase regulatory subunits. Here we demonstrate that a Medicago CYCLINT (CYCT) protein is a specific interactor of Ms;CDKC;1 and the interaction between these two proteins gives rise to an active kinase complex that localizes to the nucleus and phosphorylates the carboxy-terminal YSPTSPS heptapeptide repeat domain (CTD) of the largest subunit of RNA polymerase II in vitro. Mutation of Ser to Ala at position 5 within the heptapeptide repeat abolishes substrate phosphorylation by the Ms;CDKC;1 kinase complex. Furthermore, our data show that addition of the Medicago CDKC;1-CYCT;1 heterodimer completely restored the transcriptional activity of a HeLa nuclear extract depleted of endogeneous CDK9 kinase complexes. Together, these results indicate that the Medicago CDKC;1-CYCT;1 complex is a positive regulator of transcription in plants and has a role similar to the CDK9/cyclin T complex of human positive transcription elongation factor P-TEFb.}, language = {en}, number = {6}, urldate = {2021-06-11}, journal = {The Plant Journal}, author = {Fülöp, Katalin and Pettkó-Szandtner, Aladàr and Magyar, Zoltán and Miskolczi, Pál and Kondorosi, Éva and Dudits, Dénes and Bakó, László}, year = {2005}, note = {\_eprint: https://onlinelibrary.wiley.com/doi/pdf/10.1111/j.1365-313X.2005.02421.x}, keywords = {CDK-cyclin complex, CTD kinase, Medicago, P-TEFb, cell cycle, transcription}, pages = {810--820}, }
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@article{magyar_role_2005, title = {The {Role} of the {Arabidopsis} {E2FB} {Transcription} {Factor} in {Regulating} {Auxin}-{Dependent} {Cell} {Division}}, volume = {17}, issn = {1040-4651}, url = {https://doi.org/10.1105/tpc.105.033761}, doi = {10/dtpwks}, abstract = {The molecular mechanisms by which the phytohormone auxin coordinates cell division with cell growth and differentiation are largely unknown. Here, we show that in Arabidopsis thaliana E2FB, accumulation and stability are positively regulated by auxin. Coexpression of E2FB, but not of E2FA, with its dimerization partner A, stimulated cell proliferation in the absence of auxin in tobacco (Nicotiana tabacum) Bright Yellow-2 cells. E2FB regulated the entry into both S- and M-phases, the latter corresponding to the activation of a plant-specific mitotic regulator, CDKB1;1. Increased E2FB levels led to shortened cell cycle duration, elevated cell numbers, and extremely small cell sizes. In the absence of auxin, cells elongated with concomitant increase in their ploidy level, but both were strongly inhibited by E2FB. We conclude that E2FB is one of the key targets for auxin to determine whether cells proliferate or whether they exit the cell cycle, enlarge, and endoreduplicate their DNA.}, number = {9}, urldate = {2021-06-11}, journal = {The Plant Cell}, author = {Magyar, Zoltán and De Veylder, Lieven and Atanassova, Ana and Bakó, László and Inzé, Dirk and Bögre, László}, month = sep, year = {2005}, pages = {2527--2541}, }
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@article{espinosa-ruiz_differential_2004, title = {Differential stage-specific regulation of cyclin-dependent kinases during cambial dormancy in hybrid aspen}, volume = {38}, issn = {1365-313X}, url = {https://onlinelibrary.wiley.com/doi/abs/10.1111/j.1365-313X.2004.02070.x}, doi = {10/d4fk2f}, abstract = {The cambium of woody plants cycles between active and dormant states. Dormancy can be subdivided into eco- and endodormant stages. Ecodormant trees resume growth upon exposure to growth-promotive signals, while the establishment of endodormant state results in loss of the ability to respond to these signals. In this paper, we analysed the regulation of cyclin-dependent kinases (CDKs) to understand the differential response of cell division machinery to growth-promotive signals during the distinct stages of dormancy in hybrid aspen. We show that 4 weeks of short-day (SD) treatment causes termination of the cambial cell division and establishment of the ecodormant state. This coincides with a steady decline in the histone H1 kinase activity of the PSTAIRE-type poplar CDKA (PttCDKA) and the PPTTLRE-type PttCDKB kinase complexes. However, neither the transcript nor the polypeptide levels of PttCDKA and PttCDKB are reduced during ecodormancy. In contrast, 6 weeks of SD treatment establishes endodormancy, which is marked by the reduction and disappearance of the PttCDKA and PttCDKB protein levels and the PttCDKB transcript levels. The transition to endodormancy is preceded by an elevated E2F (adenosine E2 promoter binding factor) phosphorylation activity of the PttCDKA kinase that reduces the DNA-binding activity of E2F in vitro. The transition to endodormancy is followed by a reduction of retinoblastoma (Rb) phosphorylation activity of PttCDKA protein complexes. Both phosphorylation events could contribute to block the G1 to S phase transition upon the establishment of endodormancy. Our results indicate that eco- and endodormant stages of cambial dormancy involve a stage-specific regulation of the cell cycle effectors at multiple levels.}, language = {en}, number = {4}, urldate = {2021-06-15}, journal = {The Plant Journal}, author = {Espinosa-Ruiz, Ana and Saxena, Sangeeta and Schmidt, Julien and Mellerowicz, Ewa and Miskolczi, Pál and Bakó, László and Bhalerao, Rishikesh P.}, year = {2004}, note = {\_eprint: https://onlinelibrary.wiley.com/doi/pdf/10.1111/j.1365-313X.2004.02070.x}, keywords = {CDK regulation, cambial dormancy, cell cycle, ecodormancy, endodormancy, hybrid aspen}, pages = {603--615}, }
Paper doi link bibtex abstract
@article{meszaros_multiple_2000, title = {Multiple cyclin-dependent kinase complexes and phosphatases control {G2}/{M} progression in alfalfa cells}, volume = {43}, issn = {1573-5028}, url = {https://doi.org/10.1023/A:1006412413671}, doi = {10/cb64mn}, abstract = {Reversible phosphorylation of proteins by kinases and phosphatases plays a key regulatory role in several eukaryotic cellular functions including the control of the division cycle. Increasing numbers of sequence and biochemical data show the involvement of cyclin-dependent kinases (CDKs) and cyclins in regulation of the cell cycle progression in higher plants. The complexity represented by different types of CDKs and cyclins in a single species such as alfalfa, indicates that multicomponent regulatory pathways control G2/M transition. A set of cdc2-related genes (cdc2Ms A, B, D and F) was expressed in G2 and M cells. Phosphorylation assays also revealed that at least three kinase complexes (Cdc2Ms A/B, D and F) were successively active in G2/M cells after synchronization. Interaction between alfalfa mitotic cyclin (Medsa;CycB2;1) and a kinase partner has been reported previously. The present yeast two-hybrid analyses showed differential interaction between defined D-type cyclins and Cdc2Ms kinases functioning in G2/M phases. Localization of Cdc2Ms F kinase to the preprophase band (PPB), the perinuclear ring in early prophase, the mitotic spindle and the phragmoplast indicated a pivotal role for this kinase in mitotic plant cells. So far limited research efforts have been devoted to the functions of phosphatases in the control of plant cell division. A homologue of dual phosphatase, cdc25, has not been cloned yet from alfalfa; however tyrosine phosphorylation was indicated in the case of Cdc2Ms A kinase and the p13suc1-bound kinase activity was increased by treatment of this complex with recombinant Drosophila Cdc25. The potential role of serine/threonine phosphatases can be concluded from inhibitor studies based on okadaic acid or endothall. Endothall elevated the kinase activity of p13suc1-bound fractions in G2-phase alfalfa cells. These biochemical data are in accordance with observed cytological abnormalities. The present overview with selected original data outlines a conclusion that emphasizes the complexity of G2/M regulatory events in flowering plants.}, language = {en}, number = {5}, urldate = {2021-11-08}, journal = {Plant Molecular Biology}, author = {Mészáros, Tamás and Miskolczi, Pál and Ayaydin, Ferhan and Pettkó-Szandtner, Aladár and Peres, Adrian and Magyar, Zoltán and Horváth, Gábor V. and Bakó, László and Fehér, Attila and Dudits, Dénes}, month = aug, year = {2000}, pages = {595--605}, }
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@article{bhalerao_regulatory_1999, title = {Regulatory interaction of {PRL1} {WD} protein with {Arabidopsis} {SNF1}-like protein kinases}, volume = {96}, url = {https://www.ncbi.nlm.nih.gov/sites/ppmc/articles/PMC21862/}, doi = {10/fpvx8m}, abstract = {Mutation of the PRL1 gene, encoding a regulatory WD protein, results in glucose hypersensitivity and derepression of glucose-regulated genes in Arabidopsis. The yeast SNF1 protein kinase, a key regulator of glucose signaling, and Arabidopsis SNF1 homologs ...}, language = {en}, number = {9}, urldate = {2021-11-08}, journal = {Proceedings of the National Academy of Sciences of the United States of America}, author = {Bhalerao, Rishikesh P. and Salchert, Klaus and Bakó, László and Ökrész, László and Szabados, László and Muranaka, Toshiya and Machida, Yasunori and Schell, Jeff and Koncz, Csaba}, month = apr, year = {1999}, pmid = {10220464}, note = {Publisher: National Academy of Sciences}, pages = {5322}, }
Svenska
Vi försöker förstå de molekylära mekanismer som styr och kontrollerar sambandet mellan celldelning och celldifferentiering i växtceller.
Under vissa förutsättningar kan även en differentierad växtcell börja dela sig och, beroende på de signaler som avgör cellens framtida öde, kan de nya dottercellerna differentieras igen och ge upphov till nya organ, t ex när en stickling bildar rötter. Vi använder såväl genetiska, biokemiska som cellbiologiska metoder för att studera dessa processer på molekylär nivå.
Vi gör detta i Arabidopsis thaliana och vi undersöker de tidiga skedena när ickedelande rotpericykelceller induceras till att börja dela sig. Vi koncentrerar oss på ett protein kallat retinoblastoma relaterade proteiner (RBR), som har en viktig roll vid celldelning och celldifferentiering. Speciellt studerar vi förändringar i uttrycksmönster, hur RBR påverkar och förändrar kromatinet i kromosomerna, samt hur det fosforyleras, fördelar sig mellan olika delar i cellen och hur det bryts ned.