{tab=Research}

Laszlo Bako standing in front of a lakeIn 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.

Two pictures showing red coloured root cells of Arabidopsis.Expression of RBR-RFP fusion protein in Arabidopsis root after treatment with the auxins 2,4-D (left) or NAA (right).

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.
{tab=Team}

{tab=Publications}
  2022 (1)
ZEITLUPE Promotes ABA-Induced Stomatal Closure in Arabidopsis and Populus. Jurca, M., Sjölander, J., Ibáñez, C., Matrosova, A., Johansson, M., Kozarewa, I., Takata, N., Bakó, L., Webb, A. A. R., Israelsson-Nordström, M., & Eriksson, M. E. Frontiers in Plant Science, 13. March 2022.
ZEITLUPE Promotes ABA-Induced Stomatal Closure in Arabidopsis and Populus [link]Paper   link   bibtex   abstract  
  2021 (1)
Pickle Recruits Retinoblastoma Related 1 to Control Lateral Root Formation in Arabidopsis. Ötvös, K., Miskolczi, P., Marhavý, P., Cruz-Ramírez, A., Benková, E., Robert, S., & Bakó, L. International Journal of Molecular Sciences, 22(8): 3862. January 2021.
Pickle Recruits Retinoblastoma Related 1 to Control Lateral Root Formation in Arabidopsis [link]Paper   doi   link   bibtex   abstract   8 downloads  
  2020 (2)
Conservation analysis of core cell cycle regulators and their transcriptional behavior during limb regeneration in Ambystoma mexicanum. Espinal-Centeno, A., Dipp-Álvarez, M., Saldaña, C., Bakó, L., & Cruz-Ramírez, A. Mechanisms of Development, 164: 103651. December 2020.
Conservation analysis of core cell cycle regulators and their transcriptional behavior during limb regeneration in Ambystoma mexicanum [link]Paper   doi   link   bibtex  
The chromatin-modifying protein HUB2 is involved in the regulation of lignin composition in xylem vessels. Zhang, B., Sztojka, B., Seyfferth, C., Escamez, S., Miskolczi, P., Chantreau, M., Bakó, L., Delhomme, N., Gorzsás, A., Bhalerao, R. P., & Tuominen, H. Journal of Experimental Botany, 71(18): 5484–5494. September 2020.
The chromatin-modifying protein HUB2 is involved in the regulation of lignin composition in xylem vessels [link]Paper   doi   link   bibtex   abstract   5 downloads  
  2019 (1)
A Molecular Framework for the Control of Adventitious Rooting by TIR1/AFB2-Aux/IAA-Dependent Auxin Signaling in Arabidopsis. Lakehal, A., Chaabouni, S., Cavel, E., Le Hir, R., Ranjan, A., Raneshan, Z., Novák, O., Păcurar, D. I., Perrone, I., Jobert, F., Gutierrez, L., Bakó, L., & Bellini, C. Molecular Plant, 12(11): 1499–1514. November 2019.
A Molecular Framework for the Control of Adventitious Rooting by TIR1/AFB2-Aux/IAA-Dependent Auxin Signaling in Arabidopsis [link]Paper   doi   link   bibtex  
  2018 (2)
LEAFY activity is post-transcriptionally regulated by BLADE ON PETIOLE2 and CULLIN3 in Arabidopsis. Chahtane, H., Zhang, B., Norberg, M., LeMasson, M., Thévenon, E., Bakó, L., Benlloch, R., Holmlund, M., Parcy, F., Nilsson, O., & Vachon, G. New Phytologist, 220(2): 579–592. October 2018.
LEAFY activity is post-transcriptionally regulated by BLADE ON PETIOLE2 and CULLIN3 in Arabidopsis [link]Paper   doi   link   bibtex   1 download  
Transcriptional landscapes of Axolotl (Ambystoma mexicanum). Caballero-Pérez, J., Espinal-Centeno, A., Falcon, F., García-Ortega, L. F., Curiel-Quesada, E., Cruz-Hernández, A., Bakó, L., Chen, X., Martínez, O., Alberto Arteaga-Vázquez, M., Herrera-Estrella, L., & Cruz-Ramírez, A. Developmental Biology, 433(2): 227–239. January 2018.
Transcriptional landscapes of Axolotl (Ambystoma mexicanum) [link]Paper   doi   link   bibtex  
  2017 (2)
BLADE-ON-PETIOLE proteins act in an E3 ubiquitin ligase complex to regulate PHYTOCHROME INTERACTING FACTOR 4 abundance. Zhang, B., Holmlund, M., Lorrain, S., Norberg, M., Bakó, L., Fankhauser, C., & Nilsson, O. eLife, 6: e26759. August 2017.
BLADE-ON-PETIOLE proteins act in an E3 ubiquitin ligase complex to regulate PHYTOCHROME INTERACTING FACTOR 4 abundance [link]Paper   doi   link   bibtex   abstract  
XYLEM NAC DOMAIN1, an angiosperm NAC transcription factor, inhibits xylem differentiation through conserved motifs that interact with RETINOBLASTOMA‐RELATED. Zhao, C., Lasses, T., Bakó, L., Kong, D., Zhao, B., Chanda, B., Bombarely, A., Cruz‐Ramírez, A., Scheres, B., Brunner, A. M., & Beers, E. P. New Phytologist, 216(1): 76–89. October 2017.
XYLEM NAC DOMAIN1, an angiosperm NAC transcription factor, inhibits xylem differentiation through conserved motifs that interact with RETINOBLASTOMA‐RELATED [link]Paper   doi   link   bibtex  
  2016 (1)
The Role of microRNAs in Animal Cell Reprogramming. Cruz-Santos, M. C., Aragón-Raygoza, A., Espinal-Centeno, A., Arteaga-Vázquez, M., Cruz-Hernández, A., Bakó, L., & Cruz-Ramírez, A. Stem Cells and Development, 25(14): 1035–1049. July 2016.
The Role of microRNAs in Animal Cell Reprogramming [link]Paper   doi   link   bibtex  
  2013 (1)
ABCG9, ABCG11 and ABCG14 ABC transporters are required for vascular development in Arabidopsis. Le Hir, R., Sorin, C., Chakraborti, D., Moritz, T., Schaller, H., Tellier, F., Robert, S., Morin, H., Bakó, L., & Bellini, C. The Plant Journal, 76(5): 811–824. December 2013.
ABCG9, ABCG11 and ABCG14 ABC transporters are required for vascular development in Arabidopsis [link]Paper   doi   link   bibtex  
  2012 (4)
A Bistable Circuit Involving SCARECROW-RETINOBLASTOMA Integrates Cues to Inform Asymmetric Stem Cell Division. Cruz-Ramírez, A., Díaz-Triviño, S., Blilou, I., Grieneisen, V., Sozzani, R., Zamioudis, C., Miskolczi, P., Nieuwland, J., Benjamins, R., Dhonukshe, P., Caballero-Pérez, J., Horvath, B., Long, Y., Mähönen, A., Zhang, H., Xu, J., Murray, J., Benfey, P., Bakó, L., Marée, A., & Scheres, B. Cell, 150(5): 1002–1015. August 2012.
A Bistable Circuit Involving SCARECROW-RETINOBLASTOMA Integrates Cues to Inform Asymmetric Stem Cell Division [link]Paper   doi   link   bibtex  
Arabidopsis E2FA stimulates proliferation and endocycle separately through RBR-bound and RBR-free complexes. Magyar, Z., Horváth, B., Khan, S., Mohammed, B., Henriques, R., De Veylder, L., Bakó, L., Scheres, B., & Bögre, L. The EMBO Journal, 31(6): 1480–1493. March 2012. Publisher: John Wiley & Sons, Ltd
Arabidopsis E2FA stimulates proliferation and endocycle separately through RBR-bound and RBR-free complexes [link]Paper   doi   link   bibtex   abstract  
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. Shaikhali, J., de Dios Barajas-Lopéz, J., Ötvös, K., Kremnev, D., Garcia, A. S., Srivastava, V., Wingsle, G., Bakó, L., & Strand, Å. The Plant Cell, 24(7): 3009–3025. July 2012.
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 [link]Paper   doi   link   bibtex   2 downloads  
Use of the Foot-and-Mouth Disease Virus 2A Peptide Co-Expression System to Study Intracellular Protein Trafficking in Arabidopsis. Burén, S., Ortega-Villasante, C., Ötvös, K., Samuelsson, G., Bakó, L., & Villarejo, A. PLoS ONE, 7(12): e51973. December 2012.
Use of the Foot-and-Mouth Disease Virus 2A Peptide Co-Expression System to Study Intracellular Protein Trafficking in Arabidopsis [link]Paper   doi   link   bibtex  
  2011 (5)
Activity-dormancy transition in the cambial meristem involves stage-specific modulation of auxin response in hybrid aspen. Baba, K., Karlberg, A., Schmidt, J., Schrader, J., Hvidsten, T. R., Bakó, L., & Bhalerao, R. P. Proceedings of the National Academy of Sciences, 108(8): 3418–3423. February 2011.
Activity-dormancy transition in the cambial meristem involves stage-specific modulation of auxin response in hybrid aspen [link]Paper   doi   link   bibtex  
Immunodetection of retinoblastoma-related protein and its phosphorylated form in interphase and mitotic alfalfa cells. Abraham, E., Miskolczi, P., Ayaydin, F., Yu, P., Kotogany, E., Bakó, L., Otvos, K., Horvath, G. V., & Dudits, D. Journal of Experimental Botany, 62(6): 2155–2168. March 2011.
Immunodetection of retinoblastoma-related protein and its phosphorylated form in interphase and mitotic alfalfa cells [link]Paper   doi   link   bibtex  
Importance of Post-Translational Modifications for Functionality of a Chloroplast-Localized Carbonic Anhydrase (CAH1) in Arabidopsis thaliana. Burén, S., Ortega-Villasante, C., Blanco-Rivero, A., Martínez-Bernardini, A., Shutova, T., Shevela, D., Messinger, J., Bakó, L., Villarejo, A., & Samuelsson, G. PLoS ONE, 6(6): e21021. June 2011.
Importance of Post-Translational Modifications for Functionality of a Chloroplast-Localized Carbonic Anhydrase (CAH1) in Arabidopsis thaliana [link]Paper   doi   link   bibtex  
Partners in Time: EARLY BIRD Associates with ZEITLUPE and Regulates the Speed of the Arabidopsis Clock. Johansson, M., McWatters, H. G., Bakó, L., Takata, N., Gyula, P., Hall, A., Somers, D. E., Millar, A. J., & Eriksson, M. E. Plant Physiology, 155(4): 2108–2122. March 2011.
Partners in Time: EARLY BIRD Associates with ZEITLUPE and Regulates the Speed of the Arabidopsis Clock [link]Paper   doi   link   bibtex   abstract   1 download  
Short Day–Mediated Cessation of Growth Requires the Downregulation of AINTEGUMENTALIKE1 Transcription Factor in Hybrid Aspen. Karlberg, A., Bakó, L., & Bhalerao, R. P. PLoS Genetics, 7(11): e1002361. November 2011.
Short Day–Mediated Cessation of Growth Requires the Downregulation of AINTEGUMENTALIKE1 Transcription Factor in Hybrid Aspen [link]Paper   doi   link   bibtex  
  2010 (1)
Analysis of global changes in gene expression during activity-dormancy cycle in hybrid aspen apex. Karlberg, A., Englund, M., Petterle, A., Molnar, G., Sjödin, A., Bakó, L., & Bhalerao, R. P. Plant Biotechnology, 27(1): 1–16. 2010.
doi   link   bibtex   abstract   2 downloads  
  2006 (2)
Activation of an alfalfa cyclin-dependent kinase inhibitor by calmodulin-like domain protein kinase. Pettko-Szandtner, A., Meszaros, T., Horvath, G. V., Bakó, L., Csordas-Toth, E., Blastyak, A., Zhiponova, M., Miskolczi, P., & Dudits, D. Plant Journal, 46(1): 111–123. April 2006. Place: Hoboken Publisher: Wiley WOS:000236035700008
doi   link   bibtex   abstract  
EBP1 regulates organ size through cell growth and proliferation in plants. Horváth, B. M, Magyar, Z., Zhang, Y., Hamburger, A. W, Bakó, L., Visser, R. G., Bachem, C. W., & Bögre, L. The EMBO Journal, 25(20): 4909–4920. October 2006. Publisher: John Wiley & Sons, Ltd
EBP1 regulates organ size through cell growth and proliferation in plants [link]Paper   doi   link   bibtex   abstract  
  2005 (4)
Arabidopsis Anaphase-Promoting Complexes: Multiple Activators and Wide Range of Substrates Might Keep APC Perpetually Busy. Fülöp, K., Tarayre, S., Kelemen, Z., Horváth, G., Kevei, Z., Nikovics, K., Bakó, L., Brown, S., Kondorosi, A., & Kondorosi, E. Cell Cycle, 4(8): 4084–4092. August 2005.
Arabidopsis Anaphase-Promoting Complexes: Multiple Activators and Wide Range of Substrates Might Keep APC Perpetually Busy [link]Paper   doi   link   bibtex   abstract  
Evidence for a protein transported through the secretory pathway en route to the higher plant chloroplast. Villarejo, A., Burén, S., Larsson, S., Déjardin, A., Monné, M., Rudhe, C., Karlsson, J., Jansson, S., Lerouge, P., Rolland, N., von Heijne, G., Grebe, M., Bakó, L., & Samuelsson, G. Nature Cell Biology, 7(12): 1224–1231. December 2005. Number: 12 Publisher: Nature Publishing Group
Evidence for a protein transported through the secretory pathway en route to the higher plant chloroplast [link]Paper   doi   link   bibtex   abstract  
The Medicago CDKC;1-CYCLINT;1 kinase complex phosphorylates the carboxy-terminal domain of RNA polymerase II and promotes transcription. Fülöp, K., Pettkó-Szandtner, A., Magyar, Z., Miskolczi, P., Kondorosi, É., Dudits, D., & Bakó, L. The Plant Journal, 42(6): 810–820. 2005. _eprint: https://onlinelibrary.wiley.com/doi/pdf/10.1111/j.1365-313X.2005.02421.x
The Medicago CDKC;1-CYCLINT;1 kinase complex phosphorylates the carboxy-terminal domain of RNA polymerase II and promotes transcription [link]Paper   doi   link   bibtex   abstract  
The Role of the Arabidopsis E2FB Transcription Factor in Regulating Auxin-Dependent Cell Division. Magyar, Z., De Veylder, L., Atanassova, A., Bakó, L., Inzé, D., & Bögre, L. The Plant Cell, 17(9): 2527–2541. September 2005.
The Role of the Arabidopsis E2FB Transcription Factor in Regulating Auxin-Dependent Cell Division [link]Paper   doi   link   bibtex   abstract  
  2004 (1)
Differential stage-specific regulation of cyclin-dependent kinases during cambial dormancy in hybrid aspen. Espinosa-Ruiz, A., Saxena, S., Schmidt, J., Mellerowicz, E., Miskolczi, P., Bakó, L., & Bhalerao, R. P. The Plant Journal, 38(4): 603–615. 2004. _eprint: https://onlinelibrary.wiley.com/doi/pdf/10.1111/j.1365-313X.2004.02070.x
Differential stage-specific regulation of cyclin-dependent kinases during cambial dormancy in hybrid aspen [link]Paper   doi   link   bibtex   abstract  
  2000 (1)
Multiple cyclin-dependent kinase complexes and phosphatases control G2/M progression in alfalfa cells. Mészáros, T., Miskolczi, P., Ayaydin, F., Pettkó-Szandtner, A., Peres, A., Magyar, Z., Horváth, G. V., Bakó, L., Fehér, A., & Dudits, D. Plant Molecular Biology, 43(5): 595–605. August 2000.
Multiple cyclin-dependent kinase complexes and phosphatases control G2/M progression in alfalfa cells [link]Paper   doi   link   bibtex   abstract  
  1999 (1)
Regulatory interaction of PRL1 WD protein with Arabidopsis SNF1-like protein kinases. Bhalerao, R. P., Salchert, K., Bakó, L., Ökrész, L., Szabados, L., Muranaka, T., Machida, Y., Schell, J., & Koncz, C. Proceedings of the National Academy of Sciences of the United States of America, 96(9): 5322. April 1999. Publisher: National Academy of Sciences
Regulatory interaction of PRL1 WD protein with Arabidopsis SNF1-like protein kinases [link]Paper   doi   link   bibtex   abstract   2 downloads  
{tab=Svenska} Laszlo Bako som står framför en sjö

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.