Developmental cues are encoded by the combinatorial phosphorylation of Arabidopsis RETINOBLASTOMA-RELATED protein RBR1.

Cell Death Cell Division LXCXE Motif RBR Phosphorylation RETINOBLASTOMA-RELATED

Journal

The EMBO journal
ISSN: 1460-2075
Titre abrégé: EMBO J
Pays: England
ID NLM: 8208664

Informations de publication

Date de publication:
28 Oct 2024
Historique:
received: 22 12 2021
accepted: 27 09 2024
revised: 29 08 2024
medline: 29 10 2024
pubmed: 29 10 2024
entrez: 29 10 2024
Statut: aheadofprint

Résumé

RETINOBLASTOMA-RELATED (RBR) proteins orchestrate cell division, differentiation, and survival in response to environmental and developmental cues through protein-protein interactions that are governed by multisite phosphorylation. Here we explore, using a large collection of transgenic RBR phosphovariants to complement protein function in Arabidopsis thaliana, whether differences in the number and position of RBR phosphorylation events cause a diversification of the protein's function. While the number of point mutations influence phenotypic strength, phosphosites contribute differentially to distinct phenotypes. RBR pocket domain mutations associate primarily with cell proliferation, while mutations in the C-region are linked to stem cell maintenance. Both phospho-mimetic and a phospho-defective variants promote cell death, suggesting that distinct mechanisms can lead to similar cell fates. We observed combinatorial effects between phosphorylated T406 and phosphosites in different protein domains, suggesting that specific, additive, and combinatorial phosphorylation events fine-tune RBR function. Suppression of dominant phospho-defective RBR phenotypes with a mutation that inhibits RBR interacting with LXCXE motifs, and an exhaustive protein-protein interaction assay, not only revealed the importance of DREAM complex members in phosphorylation-regulated RBR function but also pointed to phosphorylation-independent RBR roles in environmental responses. Thus, combinatorial phosphorylation defined and separated developmental, but not environmental, functions of RBR.

Identifiants

pubmed: 39468281
doi: 10.1038/s44318-024-00282-3
pii: 10.1038/s44318-024-00282-3
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : Consejo Nacional de Humanidades, Ciencias y Tecnologías (Conahcyt)
ID : 383871

Informations de copyright

© 2024. The Author(s).

Références

Ach RA, Durfee T, Miller AB, Taranto P, Hanley-Bowdoin L, Zambryski PC, Gruissem W (1997) RRB1 and RRB2 encode maize retinoblastoma-related proteins that interact with a plant D-type cyclin and geminivirus replication protein. Mol Cell Biol 17:5077–5086
pubmed: 9271385 pmcid: 232358 doi: 10.1128/MCB.17.9.5077
Andersen SU, Algreen-Petersen RG, Hoedl M, Jurkiewicz A, Cvitanich C, Braunschweig U, Schauser L, Oh SA, Twell D, Jensen EØ (2007) The conserved cysteine-rich domain of a tesmin/TSO1-like protein binds zinc in vitro and TSO1 is required for both male and female fertility in Arabidopsis thaliana. J Exp Bot 58:3657–3670
pubmed: 18057042 doi: 10.1093/jxb/erm215
Antonucci LA, Egger JV, Krucher NA (2014) Phosphorylation of the Retinoblastoma protein (RB) on serine-807 is required for association with Bax. Cell Cycle 13:3611–3617
pubmed: 25483096 pmcid: 4614104 doi: 10.4161/15384101.2014.964093
Appel HM, Cocroft RB (2014) Plants respond to leaf vibrations caused by insect herbivore chewing. Oecologia 175:1257–1266
pubmed: 24985883 pmcid: 4102826 doi: 10.1007/s00442-014-2995-6
Barrientes S, Cooke C, Goodrich DW (2000) Glutamic acid mutagenesis of retinoblastoma protein phosphorylation sites has diverse effects on function. Oncogene 19:562–570
pubmed: 10698526 doi: 10.1038/sj.onc.1203332
Bertolotti G, Unterholzner SJ, Scintu D, Salvi E, Svolacchia N, Di Mambro R, Ruta V, Linhares Scaglia F, Vittorioso P, Sabatini S et al (2020) A PHABULOSA-controlled genetic pathway regulates ground tissue patterning in the Arabidopsis root. Curr Biol 31:1–7
Biedermann S, Harashima H, Chen P, Heese M, Bouyer D, Sofroni K, Schnittger A (2017) The retinoblastoma homolog RBR1 mediates localization of the repair protein RAD51 to DNA lesions in Arabidopsis. EMBO J 36:1279–1297
pubmed: 28320735 pmcid: 5412766 doi: 10.15252/embj.201694571
Borghi L, Gutzat R, Fütterer J, Laizet Y, Hennig L, Gruissem W (2010) Arabidopsis RETINOBLASTOMA-RELATED is required for stem cell maintenance, cell differentiation, and lateral organ production. Plant Cell 22:1792–1811
pubmed: 20525851 pmcid: 2910961 doi: 10.1105/tpc.110.074591
Bourgo RJ, Thangavel C, Ertel A, Bergseid J, Kathleen McClendon A, Wilkens L, Witkiewicz AK, Wang JYJ, Knudsen ES (2011) RB restricts DNA damage-initiated tumorigenesis through an LXCXE-dependent mechanism of transcriptional control. Mol Cell 43:663–672
pubmed: 21855804 pmcid: 4271833 doi: 10.1016/j.molcel.2011.06.029
Brown VD, Phillips RA, Gallie BL (1999) Cumulative effect of phosphorylation of pRB on regulation of E2F activity. Mol Cell Biol 19:3246–3256
pubmed: 10207050 pmcid: 84119 doi: 10.1128/MCB.19.5.3246
Burke JR, Deshong AJ, Pelton JG, Rubin SM (2010) Phosphorylation-induced conformational changes in the retinoblastoma protein inhibit E2F transactivation domain binding. J Biol Chem 285:16286–16293
pubmed: 20223825 pmcid: 2871496 doi: 10.1074/jbc.M110.108167
Burke JR, Hura GL, Rubin SM (2012) Structures of inactive retinoblastoma protein reveal multiple mechanisms for cell cycle control. Genes Dev 26:1156–1166
pubmed: 22569856 pmcid: 3371405 doi: 10.1101/gad.189837.112
Burke JR, Liban TJ, Restrepo T, Lee HW, Rubin SM (2014) Multiple mechanisms for E2F binding inhibition by phosphorylation of the retinoblastoma protein C-terminal domain. J Mol Biol 426:245–255
pubmed: 24103329 doi: 10.1016/j.jmb.2013.09.031
Chen H, Hwang JE, Lim CJ, Kim DY, Lee SY, Lim CO (2010) Arabidopsis DREB2C functions as a transcriptional activator of HsfA3 during the heat stress response. Biochem Biophys Res Commun 401:238–244
pubmed: 20849812 doi: 10.1016/j.bbrc.2010.09.038
Chen P, Takatsuka H, Takahashi N, Kurata R, Fukao Y, Kobayashi K, Ito M, Umeda M (2017) Arabidopsis R1R2R3-Myb proteins are essential for inhibiting cell division in response to DNA damage. Nat Commun 8:1–12
Chen T, Wang JYJ (2000) Establishment of irreversible growth arrest in myogenic differentiation requires the RB LXCXE-binding function. Mol Cell Biol 20:5571–5580
pubmed: 10891495 pmcid: 86015 doi: 10.1128/MCB.20.15.5571-5580.2000
Chen Z, Higgins JD, Hui JTL, Li J, Franklin FCH, Berger F (2011) Retinoblastoma protein is essential for early meiotic events in Arabidopsis. EMBO J 30:744–755
pubmed: 21217641 pmcid: 3041947 doi: 10.1038/emboj.2010.344
Cheng Y, Cao L, Wang S, Li Y, Shi X, Liu H, Li L, Zhang Z, Fowke LC, Wang H et al (2015) Downregulation of multiple CDK inhibitor ICK/KRP genes upregulates the E2F pathway and increases cell proliferation, and organ and seed sizes in Arabidopsis. Plant J 75:642–655
doi: 10.1111/tpj.12228
Christians MJ, Gingerich DJ, Hua Z, Lauer TD, Vierstra RD (2012) The light-response BTB1 and BTB2 proteins assemble nuclear ubiquitin ligases that modify phytochrome B and D signaling in Arabidopsis. Plant Physiol 160:118–134
pubmed: 22732244 pmcid: 3440189 doi: 10.1104/pp.112.199109
Collins C, Dewitte W, Murray JAH (2012) D-type cyclins control cell division and developmental rate during Arabidopsis seed development. J Exp Bot 63:3571–3586
pubmed: 22412186 pmcid: 3388828 doi: 10.1093/jxb/ers015
Collins C, Maruthi MN, Jahn CE (2015) CYCD3 D-type cyclins regulate cambial cell proliferation and secondary growth in Arabidopsis. J Exp Bot 66:4595–4606
pubmed: 26022252 pmcid: 4507761 doi: 10.1093/jxb/erv218
Cruz-Ramírez A, Díaz-Triviño S, Blilou I, Grieneisen VA, Sozzani R, Zamioudis C, Miskolczi P, Nieuwland J, Benjamins R, Dhonukshe P et al (2012) A bistable circuit involving SCARECROW-RETINOBLASTOMA integrates cues to inform asymmetric stem cell division. Cell 150:1002–1015
pubmed: 22921914 pmcid: 3500399 doi: 10.1016/j.cell.2012.07.017
Cruz-Ramírez A, Diaz-trivino S, Wachsman G, Du Y, Arteaga-Vazquez M, Zhang H, Benjamins R, Blilou I, Neef AB, Chandler V et al (2013) A SCARECROW-RETINOBLASTOMA protein network controls protective quiescence in the Arabidopsis root stem cell organizer. PLoS Biol 11:e1001724
pubmed: 24302889 pmcid: 3841101 doi: 10.1371/journal.pbio.1001724
De Leon G, Sherry TC, Krucher NA (2008) Reduced expression of PNUTS leads to activation reduced expression of PNUTS leads to activation of Rb-phosphatase and caspase-mediated apoptosis. Cancer Biol Ther 7:833–841
Demesa-Arévalo E, Vielle-Calzada JP (2013) The classical arabinogalactan protein AGP18 mediates megaspore selection in Arabidopsis. Plant Cell 25:1274–1287
pubmed: 23572547 pmcid: 3663267 doi: 10.1105/tpc.112.106237
Desfeux C, Clough SJ, Bent AF (2000) Female reproductive tissues are the primary target of agrobacterium-mediated transformation by the Arabidopsis floral-dip method 1. Plant Physiol 123:895–904
pubmed: 10889238 pmcid: 59052 doi: 10.1104/pp.123.3.895
Desvoyes B, De Mendoza A, Ruiz-Trillo I, Gutierrez C (2014) Novel roles of plant RETINOBLASTOMA-RELATED (RBR) protein in cell proliferation and asymmetric cell division. J Exp Bot 65:2657–2666
pubmed: 24323507 doi: 10.1093/jxb/ert411
Desvoyes B, Gutierrez C (2020) Roles of plant retinoblastoma protein: cell cycle and beyond. EMBO J 39:1–18
doi: 10.15252/embj.2020105802
Dick FA, Rubin SM (2013) Molecular mechanisms underlying RB protein function. Nat Rev Mol Cell Biol 14:297–306
pubmed: 23594950 pmcid: 4754300 doi: 10.1038/nrm3567
Dissmeyer N, Schnittger A (2011) Use of phospho-site substitutions to analyze the biological relevance of phosphorylation events in regulatory networks. In: Dissmeyer N, Schnittger A (eds) Methods in molecular biology. Humana Press, New York, pp 93–138
Ebel C, Mariconti L, Gruissem W (2004) Plant retinoblastoma homologues control nuclear proliferation in the female gametophyte. Nature 429:776–780
pubmed: 15201912 doi: 10.1038/nature02637
Egger JV, Lane MV, Antonucci LA, Dedi B, Nancy A, Lane MV, Antonucci LA, Dedi B, Krucher NA, Zeb EMT et al (2016) Dephosphorylation of the retinoblastoma protein (Rb) inhibits cancer cell EMT via Zeb dephosphorylation of the retinoblastoma protein (Rb) inhibits cancer cell. Cancer Biol Ther 17:1197–1205
pubmed: 27645778 pmcid: 5137485 doi: 10.1080/15384047.2016.1235668
Engler C, Youles M, Gruetzner R, Ehnert TM, Werner S, Jones JDG, Patron NJ, Marillonnet S (2014) A Golden Gate modular cloning toolbox for plants. ACS Synth Biol 3:839–843
pubmed: 24933124 doi: 10.1021/sb4001504
Ghosh R, Mishra RC, Choi B, Kwon YS, Bae DW, Park SC, Jeong MJ, Bae H (2016) Exposure to sound vibrations lead to transcriptomic, proteomic and hormonal changes in arabidopsis. Sci Rep. 6:33370
pubmed: 27665921 pmcid: 5036088 doi: 10.1038/srep33370
Goodrich DW (2006) The retinoblastoma tumor-suppressor gene, the exception that proves the rule. Oncogene 25:5233–5243
pubmed: 16936742 pmcid: 2799241 doi: 10.1038/sj.onc.1209616
Grafi G, Burnett RJ, Helentjaris TIM, Larkins BA, DeCaprio JA, Sellers WR, Kaelin WG Jr (1996) A maize cDNA encoding a member of the retinoblastoma protein family: Involvement in endoreduplication. Proc Natl Acad Sci USA 93:8962–8967
pubmed: 8799136 pmcid: 38577 doi: 10.1073/pnas.93.17.8962
Gubern A, Joaquin M, Marquès M, Maseres P, Garcia-Garcia J, Amat R, González-Nuñez D, Oliva B, Real FX, de Nadal E et al (2016) The N-terminal phosphorylation of RB by p38 bypasses its inactivation by CDKs and prevents proliferation in cancer cells. Mol Cell 64:25–36
pubmed: 27642049 doi: 10.1016/j.molcel.2016.08.015
Gutierrez C (2005) Coupling cell proliferation and development in plants. Nat Cell Biol 7:535–541
pubmed: 15928697 doi: 10.1038/ncb0605-535
Gutzat R, Borghi L, Futterer J, Bischof S, Laizet Y, Hennig L, Feil R, Lunn J, Gruissem W (2011) RETINOBLASTOMA-RELATED PROTEIN controls the transition to autotrophic plant development. Development 138:2977–2986
pubmed: 21693514 doi: 10.1242/dev.060830
Gutzat R, Borghi L, Gruissem W (2012) Emerging roles of RETINOBLASTOMA-RELATED proteins in evolution and plant development. Trends Plant Sci 17:139–148
pubmed: 22240181 doi: 10.1016/j.tplants.2011.12.001
Han S, Qi X, Sugihara K, Dang JH, Endo TA, Kristen L, Kim E, Miura T, Torii KU (2018) MUTE directly orchestrates cell-state switch and the single symmetric division to create stomata. Dev Cell 45:303–315
Harashima H, Sugimoto K (2016) Integration of developmental and environmental signals into cell proliferation and differentiation through RETINOBLASTOMA-RELATED 1. Curr Opin Plant Biol 29:95–103
pubmed: 26799131 doi: 10.1016/j.pbi.2015.12.003
Horiguchi G, Tsukaya H (2011) Organ size regulation in plants: Insights from compensation. Front Plant Sci 2:1–6
doi: 10.3389/fpls.2011.00024
Horvath BM, Kourova H, Nagy S, Nemeth E, Magyar Z, Papdi C, Ahmad Z, Sanchez-perez GF, Perilli S, Blilou I et al (2017) Arabidopsis RETINOBLASTOMA RELATED directly regulates DNA damage responses through functions beyond cell cycle control. EMBO J 36:1261–1278
pubmed: 28320736 pmcid: 5412863 doi: 10.15252/embj.201694561
Hu X, Kong X, Wang C, Ma L, Zhao J, Wei J, Zhang X, Loake GJ, Zhang T, Huang J et al (2014) Proteasome-mediated degradation of FRIGIDA modulates flowering time in Arabidopsis during vernalization. Plant Cell 26:4763–4781
pubmed: 25538183 pmcid: 4311208 doi: 10.1105/tpc.114.132738
Ianari A, Natale T, Calo E, Ferretti E, Alesse E, Screpanti I, Haigis K, Gulino A, Lees JA (2010) Proapoptotic function of the Retinoblastoma Tumor Suppressor protein. Cancer Cell 15:184–194
Kim HJ, Park JH, Kim J, Kim JJ, Hong S, Kim J, Kim JH, Woo HR, Hyeon C, Lim PO et al (2018) Time-evolving genetic networks reveal a nac troika that negatively regulates leaf senescence in arabidopsis. Proc Natl Acad Sci USA 115:E4930–E4939
pubmed: 29735710 pmcid: 6003463
Kim S, Choi HI, Ryu HJ, Ji HP, Myoung DK, Soo YK (2004) ARIA, an arabidopsis arm repeat protein interacting with a transcriptional regulator of abscisic acid-responsive gene expression, is a novel abscisic acid signaling component. Plant Physiol 136:3639–3648
pubmed: 15516505 pmcid: 527162 doi: 10.1104/pp.104.049189
Knudsen ES, Wang JY (1997) Dual mechanisms for the inhibition of E2F binding to RB by cyclin-dependent kinase-mediated RB phosphorylation. Mol Cell Biol 17:5771–5783
pubmed: 9315635 pmcid: 232425 doi: 10.1128/MCB.17.10.5771
Knudsen ES, Wang JYJ (1996) Differential regulation of retinoblastoma protein function by specific Cdk phosphorylation sites. J Biol Chem 271: 8313–8320
Knudsen KE, Weber E, Arden KC, Cavenee WK, Feramisco JR, Knudsen ES (1999) The retinoblastoma tumor suppressor inhibits cellular proliferation through two distinct mechanisms: Inhibition of cell cycle progression and induction of cell death. Oncogene 18:5239–5245
pubmed: 10498874 doi: 10.1038/sj.onc.1202910
Kobayashi K, Suzuki T, Iwata E, Nakamichi N, Suzuki T, Chen P, Ohtani M, Ishida T, Hosoya H, Müller S et al (2015) Transcriptional repression by MYB 3 R proteins regulates plant organ growth. EMBO J 34:1992–2007
Lang L, Pettkó-Szandtner A, Elbasi HT, Takatsuka H, Nomoto Y, Zaki A, Dorokhov S, De Jaeger G, Eeckhout D, Ito M et al (2021) The DREAM complex represses growth in response to DNA damage in Arabidopsis. Life Sci Alliance 4:1–20
doi: 10.26508/lsa.202101141
Lee HJ, Lee WK, Kang CW, Ku CR, Cho YH, Lee EJ (2018) A selective cyclin-dependent kinase 4, 6 dual inhibitor, Ribociclib (LEE011) inhibits cell proliferation and induces apoptosis in aggressive thyroid cancer. Cancer Lett 417:131–140
pubmed: 29306020 doi: 10.1016/j.canlet.2017.12.037
Lee KP, Lopez-Molina L (2013) A seed coat bedding assay to genetically explore in vitro how the endosperm controls seed germination in Arabidopsis thaliana. J Vis Exp 81:e50732
Lents NH, Gorges LL, Baldassare JJ (2006) Reverse mutational analysis reveals threonine-373 as a potentially sufficient phosphorylation site for inactivation of the retinoblastoma tumor suppressor protein (pRB). Cell Cycle 5:1699–1707
pubmed: 16880741 doi: 10.4161/cc.5.15.3126
Liu Q, Kasuga M, Sakuma Y, Abe H, Miura S, Yamaguchi-Shinozaki K, Shinozaki K (1998) Two transcription factors, DREB1 and DREB2, with an EREBP/AP2 DNA binding domain separate two cellular signal transduction pathways in drought- and low-temperature-responsive gene expression, respectively, in Arabidopsis. Plant Cell 10:1391–1406
pubmed: 9707537 pmcid: 144379 doi: 10.1105/tpc.10.8.1391
Lu G, Paul AL, McCarty DR, Ferl RJ (1996) Transcription factor veracity: Is GBF3 responsible for ABA-regulated expression of arabidopsis Adh? Plant Cell 8:847–857
pubmed: 8672884 pmcid: 161143 doi: 10.1105/tpc.8.5.847
Matos JL, Lau OS, Hachez C, Cruz-Ramírez A, Scheres B, Bergmann DC (2014) Irreversible fate commitment in the Arabidopsis stomatal lineage requires a FAMA and RETINOBLASTOMA-RELATED module. eLife 3:1–15
doi: 10.7554/eLife.03271
Menges M, De Jager SM, Gruissem W, Murray JA (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
Menkens AE, Cashmore AR (1994) Isolation and characterization of a fourth Arabidopsis thaliana G-box- binding factor, which has similarities to Fos oncoprotein. Proc Natl Acad Sci USA 91:2522–2526
pubmed: 8146148 pmcid: 43401 doi: 10.1073/pnas.91.7.2522
Munro S, Carr SM, La Thangue NB (2012) Diversity within the pRb pathway: is there a code of conduct. Oncogene 31:4343–4352
pubmed: 22249267 doi: 10.1038/onc.2011.603
Nakashima K, Shinwari ZK, Sakuma Y, Seki M, Miura S, Shinozaki K, Yamaguchi-Shinozaki K (2000) Organization and expression of two Arabidopsis DREB2 genes encoding DRE-binding proteins involved in dehydration- and high-salinity-responsive gene expression. Plant Mol Biol 42:657–665
pubmed: 10809011 doi: 10.1023/A:1006321900483
Narasimha AM, Kaulich M, Shapiro GS, Choi YJ, Sicinski P, Dowdy SF (2014) Cyclin D activates the Rb tumor suppressor by mono-phosphorylation. eLife 3:1–21
doi: 10.7554/eLife.02872
Nath N, Wang S, Betts V, Knudsen E, Chellappan S (2003) Apoptotic and mitogenic stimuli inactivate Rb by differential utilization of p38 and cyclin-dependent kinases. Oncogene 22:5986–5994
pubmed: 12955077 doi: 10.1038/sj.onc.1206843
Ning Y, Liu N, Lan K, Su Y, Li L, Chen S, He X (2020) DREAM complex suppresses DNA methylation maintenance genes and precludes DNA hypermethylation. Nat Plants 6:942–956
pubmed: 32661276 doi: 10.1038/s41477-020-0710-7
Noir S, Marrocco K, Masoud K, Thomann A, Gusti A, Bitrian M, Schnittger A, Genschik P (2015) The control of arabidopsis thaliana growth by cell proliferation and endoreplication requires the F-box protein FBL17. Plant Cell 27:1461–1476
pubmed: 25944099 pmcid: 4456641 doi: 10.1105/tpc.114.135301
Orosa B, He Q, Mesmar J, Gilroy EM, McLellan H, Yang C, Craig A, Bailey M, Zhang C, Moore JD et al (2017) BTB-BACK domain protein POB1 suppresses immune cell death by targeting ubiquitin E3 ligase PUB17 for degradation. PLoS Genet 13:1–26
doi: 10.1371/journal.pgen.1006540
Paternot S, Arsenijevic T, Dumont KJ, Roger PP (2006) Distinct specificities of pRb phosphorylation by CDK4 activated by cyclin D1 or cyclin D3: differential involvement in the distinct mitogenic modes of thyroid epithelial cells. Cell Cycle 5:61–70
Perilli S, Perez-Perez JM, Di Mambro R, Peris CL, Díaz-Triviño S, Del Bianco M, Pierdonati E, Moubayidin L, Cruz-Ramírez A, Costantino P et al (2013) RETINOBLASTOMA-RELATED protein stimulates cell differentiation in the Arabidopsis root meristem by interacting with cytokinin signaling. Plant Cell 25:4469–4478
pubmed: 24285791 pmcid: 3875730 doi: 10.1105/tpc.113.116632
Pogoda M, Liu F, Douchkov D, Djamei A, Reif JC, Schweizer P, Schulthess AW (2020) Identification of novel genetic factors underlying the host-pathogen interaction between barley (Hordeum vulgare L.) and powdery mildew (Blumeria graminis f. sp. hordei). PLoS ONE 15:1–23
doi: 10.1371/journal.pone.0235565
Pruneda-Paz JLL, Breton G, Nagel DHH, Kang SEE, Bonaldi K, Doherty CJJ, Ravelo S, Galli M, Ecker JRR, Kay SAA (2014) A genome-scale resource for the functional characterization of Arabidopsis transcription factors. Cell Rep 8:622–632
pubmed: 25043187 pmcid: 4125603 doi: 10.1016/j.celrep.2014.06.033
Rubin SM (2013) Deciphering the retinoblastoma protein phosphorylation code. Trends Biochem Sci 38:12–19
pubmed: 23218751 doi: 10.1016/j.tibs.2012.10.007
Rubin SM, Gall AL, Zheng N, Pavletich NP (2005) Structure of the Rb C-terminal domain bound to E2F1-DP1: A mechanism for phosphorylation-induced E2F release. Cell 123:1093–1106
pubmed: 16360038 doi: 10.1016/j.cell.2005.09.044
Sablowski R, Carnier Dornelas M (2014) Interplay between cell growth and cell cycle in plants. J Exp Bot 65:2703–2714
pubmed: 24218325 doi: 10.1093/jxb/ert354
Sanidas I, Morris R, Fella KA, Rumde PH, Boukhali M, Tai EC, Ting DT, Lawrence MS, Haas W, Dyson NJ (2019) A code of mono-phosphorylation modulates the function of RB. Mol Cell 73:985–1000.e6
pubmed: 30711375 pmcid: 6424368 doi: 10.1016/j.molcel.2019.01.004
Sanz L, Dewitte W, Forzani C, Patell F, Nieuwland J, Wen B, Quelhas P, de Jager S, Titmus C, Campilho A et al (2011) The Arabidopsis D-type cyclin CYCD2;1 and the inhibitor ICK2/KRP2 modulate auxin-induced lateral root formation. Plant Cell 23:641–660
pubmed: 21357490 pmcid: 3077792 doi: 10.1105/tpc.110.080002
Takahashi N, Ogita N, Takahashi T, Taniguchi S, Tanaka M, Seki M, Umeda M (2019) A regulatory module controlling stress-induced cell cycle arrest in Arabidopsis. eLife 8:1–27
doi: 10.7554/eLife.43944
Truskina J, Vernoux T (2018) The growth of a stable stationary structure: coordinating cell behavior and patterning at the shoot apical meristem. Curr Opin Plant Biol 41:83–88
pubmed: 29073502 doi: 10.1016/j.pbi.2017.09.011
Verkest A, de O Mane C-L, Vercruysse S, Maes S, Van Der Schueren E, Beeckman T, Genschik P, Kuiper M, Inze 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
pubmed: 15863515 pmcid: 1143072 doi: 10.1105/tpc.105.032383
Wachsman G, Heidstra R, Scheres B (2011) Distinct cell-autonomous functions of RETINOBLASTOMA-RELATED in Arabidopsis stem cells revealed by the brother of Brainbow Clonal analysis system. Plant Cell 23:2581–2591
pubmed: 21742994 pmcid: 3226226 doi: 10.1105/tpc.111.086199
Wang S, Gu Y, Zebell SG, Anderson LK, Wang W, Mohan R, Dong X (2014a) A noncanonical role for the CKI-RB-E2F cell-cycle signaling pathway in plant effector-triggered immunity. Cell Host Microbe 16:787–794
pubmed: 25455564 pmcid: 4282163 doi: 10.1016/j.chom.2014.10.005
Wang W, Zhang J, Qin Q (2014b) The six conserved serine/threonine sites of REPRESSOR OF ga1 - 3 protein are important for its functionality and stability in gibberellin signaling in Arabidopsis. Planta 240:763–779
Weimer AK, Biedermann S, Harashima H, Roodbarkelari F, Takahashi N, Foreman J, Guan Y, Pochon G, Heese M, Van Damme D et al (2016) The plant‐specific CDKB 1‐ CYCB 1 complex mediates homologous recombination repair in Arabidopsis. EMBO J 35:2068–2086
pubmed: 27497297 pmcid: 5048351 doi: 10.15252/embj.201593083
Weimer AK, Matos JL, Sharma N, Patell F, Murray JAH, Dewitte W, Bergmann DC (2018) Lineage- and stage-specific expressed CYCD7;1 coordinates the single symmetric division that creates stomatal guard cells. Development 145:dev160671
pubmed: 29467245 pmcid: 5897600 doi: 10.1242/dev.160671
Wen B, Nieuwland J, Murray JAH (2013) The Arabidopsis CDK inhibitor ICK3/KRP5 is rate limiting for primary root growth and promotes growth through cell elongation and endoreduplication. J Exp Bot 64:1135–1144
pubmed: 23440171 doi: 10.1093/jxb/ert009
Wildwater M, Campilho A, Perez-Perez JM, Heidstra R, Blilou I, Korthout H, Chatterjee J, Mariconti L, Gruissem W, Scheres B (2005) The RETINOBLASTOMA-RELATED gene regulates stem cell maintenance in Arabidopsis roots. Cell 123:1337–1349
pubmed: 16377572 doi: 10.1016/j.cell.2005.09.042
Willems A, Heyman J, Eekhout T, Achon I, Pedroza-Garcia JA, Zhu T, Li L, Vercauteren I, Van den Daele H, van de Cotte B et al (2020) The cyclin CYCA3;4 is a postprophase target of the APC/CCCS52A2 E3-ligase controlling formative cell divisions in Arabidopsis. Plant Cell 32:2979–2996
pubmed: 32690720 pmcid: 7474283 doi: 10.1105/tpc.20.00208
Xie Q, Sanz-Burgos AP, Hannon GJ, Gutiérrez C (1996) Plant cells contain a novel member of the retinoblastoma family of growth regulatory proteins. EMBO J 15:4900–4908
pubmed: 8890163 pmcid: 452227 doi: 10.1002/j.1460-2075.1996.tb00870.x
Yi D, Kamei CLA, Cools T, Vanderauwera S, Takahashi N, Okushima Y, Eekhout T, Yoshiyama KO, Larkin J, Van den Daele H et al (2014) The Arabidopsis SIAMESE-RELATED cyclin-dependent kinase inhibitors SMR5 and SMR7 regulate the DNA damage checkpoint in response to reactive oxygen species. Plant Cell 26:296–309
pubmed: 24399300 pmcid: 3963576 doi: 10.1105/tpc.113.118943
Zhao X, Bramsiepe J, Van Durme M, Komaki S, Prusicki MA, Maruyama D, Forner J, Medzihradszky A, Wijnker E, Harashima H et al (2017) RETINOBLASTOMA RELATED1 mediates germline entry in Arabidopsis. Science 356:eaaf6532
Zhou W, Lozano-Torres JL, Blilou I, Zhang X, Zhai Q, Smant G, Li C, Scheres B (2019) A jasmonate signaling network activates root stem cells and promotes regeneration. Cell 177:942–956.e14
pubmed: 30955889 doi: 10.1016/j.cell.2019.03.006

Auteurs

Jorge Zamora-Zaragoza (J)

Laboratory of Cell and Developmental Biology, Department of Plant Sciences, Wageningen University and Research, 6708 PB, Wageningen, The Netherlands.
Rijk Zwaan Breeding B.V., Department of Biotechnology, Eerste Kruisweg 9, 4793 RS, Fijnaart, The Netherlands.

Katinka Klap (K)

Laboratory of Cell and Developmental Biology, Department of Plant Sciences, Wageningen University and Research, 6708 PB, Wageningen, The Netherlands.

Jaheli Sánchez-Pérez (J)

Laboratorio Nacional de Genómica para la Biodiversidad, Centro de Investigación y de Estudios Avanzados del Instituto Politécnico Nacional, 36824, Irapuato, Guanajuato, Mexico.

Jean-Philippe Vielle-Calzada (JP)

Laboratorio Nacional de Genómica para la Biodiversidad, Centro de Investigación y de Estudios Avanzados del Instituto Politécnico Nacional, 36824, Irapuato, Guanajuato, Mexico.

Viola Willemsen (V)

Laboratory of Cell and Developmental Biology, Department of Plant Sciences, Wageningen University and Research, 6708 PB, Wageningen, The Netherlands.

Ben Scheres (B)

Laboratory of Cell and Developmental Biology, Department of Plant Sciences, Wageningen University and Research, 6708 PB, Wageningen, The Netherlands. ben.scheres@wur.nl.
Rijk Zwaan Breeding B.V., Department of Biotechnology, Eerste Kruisweg 9, 4793 RS, Fijnaart, The Netherlands. ben.scheres@wur.nl.

Classifications MeSH