Abstract
Main conclusion
This study unravels a novel regulatory module (CRL4-CK2α-CDK2) involving fruit size control by mediating cell division homeostasis (SlCK2α and SlCDK2) in tomato.
Abstract
Fruit size is one of the crucial agronomical traits for crop production. UV-damaged DNA binding protein 1 (DDB1), a core component of Cullin4-RING E3 ubiquitin ligase complex (CRL4), has been identified as a negative regulator of fruit size in tomato (Solanum lycopersicum). However, the underlying molecular mechanism remains largely unclear. Here, we report the identification and characterization of a SlDDB1-interacting protein putatively involving fruit size control through regulating cell proliferation in tomato. It is a tomato homolog SlCK2α, the catalytic subunit of the casein kinase 2 (CK2), identified by yeast two-hybrid (Y2H) assays. The interaction between SlDDB1 and SlCK2α was demonstrated by bimolecular fluorescence complementation (BiFC) and co-immunoprecipitation (Co-IP). RNA interference (RNAi) and CRISPR/Cas9-based mutant analyses showed that lack of SlCK2α resulted in reduction of fruit size with reduced cell number, suggesting it is a positive regulator on fruit size by promoting cell proliferation. We also showed SlDDB1 is required to ubiquitinate SlCK2α and negatively regulate its stability through 26S proteasome-mediated degradation. Furthermore, we found that a tomato homolog of cell division protein kinase 2 (SlCDK2) could interact with and specifically be phosphorylated by SlCK2α, resulting in an increase of SlCDK2 protein stability. CRISPR/Cas9-based genetic evidence showed that SlCDK2 is also a positive regulator of fruit size by influencing cell division in tomato. Taken together, our findings, thus, unravel a novel regulatory module CRL4-CK2α-CDK2 in finely modulating cell division homeostasis and the consequences on fruit size.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
All data generated from the study appear in the submitted article.
Abbreviations
- BiFC:
-
Bimolecular fluorescence complementation
- CDK2:
-
Cell division protein kinase 2
- CK2:
-
Casein kinase 2
- Co-IP:
-
Co-immunoprecipitation
- CRL4:
-
Cullin4-RING E3 ubiquitin ligase complex
- DAP:
-
Days after pollination
- DDB1:
-
UV-damaged DNA binding protein 1
- Y2H:
-
Yeast two-hybrid
References
Adachi S, Nobusawa T, Umeda M (2009) Quantitative and cell type-specific transcriptional regulation of A-type cyclin-dependent kinase in Arabidopsis thaliana. Dev Biol 329:306–314. https://doi.org/10.1016/j.ydbio.2009.03.002
Aihara Y, Fujimura-Kamada K, Yamasaki T, Minagawa J (2019) Algal photoprotection is regulated by the E3 ligase CUL4-DDB1DET1. Nat Plants 5:34–40. https://doi.org/10.1038/s41477-018-0332-5
Al Khateeb WM, Schroeder DF (2009) Overexpression of Arabidopsis damaged DNA binding protein 1A (DDB1A) enhances UV tolerance. Plant Mol Biol 70:371–383. https://doi.org/10.1007/s11103-009-9479-9
Alpert KB, Tanksley SD (1996) High-resolution mapping and isolation of a yeast artificial chromosome contig containing fw2.2: a major fruit weight quantitative trait locus in tomato. Proc Natl Acad Sci USA 93:15503–15507. https://doi.org/10.1073/pnas.93.26.15503
Azzi L, Deluche C, Gévaudant F, Frangne N, Delmas F, Hernould M, Chevalier C (2015) Fruit growth-related genes in tomato. J Exp Bot 66:1075–1086. https://doi.org/10.1093/jxb/eru527
Beauchet A, Gévaudant F, Gonzalez N, Chevalier C (2021) In search of the still unknown function of FW2.2/CELL NUMBER REGULATOR, a major regulator of fruit size in tomato. J Exp Bot 72:5300–5311. https://doi.org/10.1093/jxb/erab207
Biedermann S, Hellmann H (2010) The DDB1a interacting proteins ATCSA-1 and DDB2 are critical factors for UV-B tolerance and genomic integrity in Arabidopsis thaliana. Plant J 62:404–415. https://doi.org/10.1111/j.1365-313X.2010.04157.x
Biedermann S, Hellmann H (2011) WD40 and CUL4-based E3 ligases: lubricating all aspects of life. Trends Plant Sci 16:38–46. https://doi.org/10.1016/j.tplants.2010.09.007
Bollier N, Sicard A, Leblond J, Latrasse D, Gonzalez N, Gévaudant F, Benhamed M, Raynaud C, Lenhard M, Chevalier C, Hernould M, Delmas F (2018) At-MINI ZINC FINGER2 and Sl-INHIBITOR OF MERISTEM ACTIVITY, a conserved missing link in the regulation of floral meristem termination in Arabidopsis and tomato. Plant Cell 30:83–100. https://doi.org/10.1105/tpc.17.00653
Bu Q, Zhu L, Dennis MD, Yu L, Lu SX, Person MD, Tobin EM, Browning KS, Huq E (2011) Phosphorylation by CK2 enhances the rapid light-induced degradation of phytochrome interacting factor 1 in Arabidopsis. J Biol Chem 286:12066–12074. https://doi.org/10.1074/jbc.M110.186882
Chakrabarti M, Zhang N, Sauvage C, Muños S, Blanca J, Cañizares J, Diez MJ, Schneider R, Mazourek M, McClead J, Causse M, van der Knaap E (2013) A cytochrome P450 regulates a domestication trait in cultivated tomato. Proc Natl Acad Sci USA 110:17125–17130. https://doi.org/10.1073/pnas.1307313110
Cheniclet C, Rong WY, Causse M, Frangne N, Bolling L, Carde J-P, Renaudin J-P (2005) Cell expansion and endoreduplication show a large genetic variability in pericarp and contribute strongly to tomato fruit growth. Plant Physiol 139:1984–1994. https://doi.org/10.1104/pp.105.068767
Chevalier C, Nafati M, Mathieu-Rivet E, Bourdon M, Frangne N, Cheniclet C, Renaudin J-P, Gévaudant F, Hernould M (2011) Elucidating the functional role of endoreduplication in tomato fruit development. Ann Bot 107:1159–1169. https://doi.org/10.1093/aob/mcq257
Chevalier C, Bourdon M, Pirrello J, Cheniclet C, Gévaudant F, Frangne N (2014) Endoreduplication and fruit growth in tomato: evidence in favour of the karyoplasmic ratio theory. J Exp Bot 65:2731–2746. https://doi.org/10.1093/jxb/ert366
Chu YH, Jang JC, Huang Z, van der Knaap E (2019) Tomato locule number and fruit size controlled by natural alleles of lc and fas. Plant Dir 3:e00142. https://doi.org/10.1002/pld3.142
Cong B, Barrero LS, Tanksley SD (2008) Regulatory change in YABBY-like transcription factor led to evolution of extreme fruit size during tomato domestication. Nat Genet 40:800–804. https://doi.org/10.1038/ng.144
Czerednik A, Busscher M, Bielen BAM, Wolters-Arts M, de Maagd RA, Angenent GC (2012) Regulation of tomato fruit pericarp development by an interplay between CDKB and CDKA1 cell cycle genes. J Exp Bot 63:2605–2617. https://doi.org/10.1093/jxb/err451
Czerednik A, Busscher M, Angenent GC, de Maagd RA (2015) The cell size distribution of tomato fruit can be changed by overexpression of CDKA1. Plant Biotechnol J 13:259–268. https://doi.org/10.1111/pbi.12268
Dang F, Nie L, Wei W (2021) Ubiquitin signaling in cell cycle control and tumorigenesis. Cell Death Differ 28:427–438. https://doi.org/10.1038/s41418-020-00648-0
Dumbliauskas E, Lechner E, Jaciubek M, Berr A, Pazhouhandeh M, Alioua M, Cognat V, Brukhin V, Koncz C, Grossniklaus U, Molinier J, Genschik P (2011) The Arabidopsis CUL4-DDB1 complex interacts with MSI1 and is required to maintain MEDEA parental imprinting. EMBO J 30:731–743. https://doi.org/10.1038/emboj.2010.359
Filhol O, Martiel J-L, Cochet C (2004) Protein kinase CK2: a new view of an old molecular complex. EMBO Rep 5:351–355. https://doi.org/10.1038/sj.embor.7400115
Frary A, Nesbitt TC, Grandillo S, Knaap E, Cong B, Liu J, Meller J, Elber R, Alpert KB, Tanksley SD (2000) fw2.2: a quantitative trait locus key to the evolution of tomato fruit size. Science 289:85–88. https://doi.org/10.1126/science.289.5476.85
Giovannoni JJ (2004) Genetic regulation of fruit development and ripening. Plant Cell 16(Suppl):S170-180. https://doi.org/10.1105/tpc.019158
Gonzalez N, Gévaudant F, Hernould M, Chevalier C, Mouras A (2007) The cell cycle-associated protein kinase WEE1 regulates cell size in relation to endoreduplication in developing tomato fruit. Plant J 51:642–655. https://doi.org/10.1111/j.1365-313X.2007.03167.x
Guo M, Simmons CR (2011) Cell number counts–the fw2.2 and CNR genes and implications for controlling plant fruit and organ size. Plant Sci 181:1–7. https://doi.org/10.1016/j.plantsci.2011.03.010
Harashima H, Dissmeyer N, Schnittger A (2013) Cell cycle control across the eukaryotic kingdom. Trends Cell Biol 23:345–356. https://doi.org/10.1016/j.tcb.2013.03.002
Hardtke CS, Gohda K, Osterlund MT, Oyama T, Okada K, Deng XW (2000) HY5 stability and activity in Arabidopsis is regulated by phosphorylation in its COP1 binding domain. EMBO J 19:4997–5006. https://doi.org/10.1093/emboj/19.18.4997
Iovine B, Iannella ML, Bevilacqua MA (2011) Damage-specific DNA binding protein 1 (DDB1): a protein with a wide range of functions. Int J Biochem Cell Biol 43:1664–1667. https://doi.org/10.1016/j.biocel.2011.09.001
Irigoyen ML, Iniesto E, Rodriguez L, Puga MI, Yanagawa Y, Pick E, Strickland E, Paz-Ares J, Wei N, de Jaeger G, Rodriguez PL, Deng XW, Rubio V (2014) Targeted degradation of abscisic acid receptors is mediated by the ubiquitin ligase substrate adaptor DDA1 in Arabidopsis. Plant Cell 26:712–728. https://doi.org/10.1105/tpc.113.122234
Iwakawa H, Shinmyo A, Sekine M (2006) Arabidopsis CDKA;1, a cdc2 homologue, controls proliferation of generative cells in male gametogenesis. Plant J 45:819–831. https://doi.org/10.1111/j.1365-313X.2005.02643.x
Joubès J, Phan TH, 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. https://doi.org/10.1104/pp.121.3.857
Joubès J, Chevalier C, Dudits D, Heberle-Bors E, Inzé D, Umeda M, Renaudin JP (2000) CDK-related protein kinases in plants. Plant Mol Biol 43:607–620. https://doi.org/10.1023/a:1006470301554
Kang HG, Klessig DF (2005) Salicylic acid-inducible Arabidopsis CK2-like activity phosphorylates TGA2. Plant Mol Biol 57:541–557. https://doi.org/10.1007/s11103-005-0409-1
Komaki S, Sugimoto K (2012) Control of the plant cell cycle by developmental and environmental cues. Plant Cell Physiol 53:953–964. https://doi.org/10.1093/pcp/pcs070
Li P, Liu J (2021) Protein phosphorylation in plant cell signaling. Methods Mol Biol 2358:45–71. https://doi.org/10.1007/978-1-0716-1625-3_3
Li Y, Zhang J, Gao W, Zhang L, Pan Y, Zhang S, Wang Y (2015) Insights on structural characteristics and ligand binding mechanisms of CDK2. Int J Mol Sci 16:9314–9340. https://doi.org/10.3390/ijms16059314
Li Y, Deng H, Miao M, Li H, Huang S, Wang S, Liu Y (2016) Tomato MBD5, a methyl CpG binding domain protein, physically interacting with UV-damaged DNA binding protein-1, functions in multiple processes. New Phytol 210:208–226. https://doi.org/10.1111/nph.13745
Litchfield DW (2003) Protein kinase CK2: structure, regulation and role in cellular decisions of life and death. Biochem J 369:1–15. https://doi.org/10.1042/BJ20021469
Liu J, van Eck J, Cong B, Tanksley SD (2002) A new class of regulatory genes underlying the cause of pear-shaped tomato fruit. Proc Natl Acad Sci USA 99:13302–13306. https://doi.org/10.1073/pnas.162485999
Liu Y, Roof S, Ye Z, Barry C, van Tuinen A, Vrebalov J, Bowler C, Giovannoni J (2004) Manipulation of light signal transduction as a means of modifying fruit nutritional quality in tomato. Proc Natl Acad Sci USA 101:9897–9902. https://doi.org/10.1073/pnas.0400935101
Liu J, Tang X, Gao L, Gao Y, Li Y, Huang S, Sun X, Miao M, Zeng H, Tian X, Niu X, Zheng L, Giovannoni J, Xiao F, Liu Y (2012) A role of tomato UV-damaged DNA binding protein 1 (DDB1) in organ size control via an epigenetic manner. PLoS ONE 7:e42621. https://doi.org/10.1371/journal.pone.0042621
Lu SX, Liu H, Knowles SM, Li J, Ma L, Tobin EM, Lin C (2011) A role for protein kinase casein kinase2 α-subunits in the Arabidopsis circadian clock. Plant Physiol 157:1537–1545. https://doi.org/10.1104/pp.111.179846
Mariotti L, Picciarelli P, Lombardi L, Ceccarelli N (2011) Fruit-set and early fruit growth in tomato are associated with increases in indoleacetic acid, cytokinin, and bioactive gibberellin contents. J Plant Growth Regul 30:405–415. https://doi.org/10.1007/s00344-011-9204-1
Mathieu-Rivet E, Gévaudant F, Sicard A, Salar S, Do PT, Mouras A, Fernie AR, Gibon Y, Rothan C, Chevalier C, Hernould M (2010) Functional analysis of the anaphase promoting complex activator CCS52A highlights the crucial role of endo-reduplication for fruit growth in tomato. Plant J 62:727–741. https://doi.org/10.1111/j.1365-313X.2010.04198.x
Mauxion J-P, Chevalier C, Gonzalez N (2021) Complex cellular and molecular events determining fruit size. Trends Plant Sci 26:1023–1038. https://doi.org/10.1016/j.tplants.2021.05.008
Meggio F, Pinna LA (2003) One-thousand-and-one substrates of protein kinase CK2? FASEB J 17:349–368. https://doi.org/10.1096/fj.02-0473rev
Miao M, Zhu Y, Qiao M, Tang X, Zhao W, Xiao F, Liu Y (2014) The tomato DWD motif-containing protein DDI1 interacts with the CUL4-DDB1-based ubiquitin ligase and plays a pivotal role in abiotic stress responses. Biochem Biophys Res Commun 450:1439–1445. https://doi.org/10.1016/j.bbrc.2014.07.011
Molinier J, Lechner E, Dumbliauskas E, Genschik P (2008) Regulation and role of Arabidopsis CUL4-DDB1A-DDB2 in maintaining genome integrity upon UV stress. PLoS Genet 4:e1000093. https://doi.org/10.1371/journal.pgen.1000093
Moreno-Romero J, Armengot L, Marquès-Bueno MM, Cadavid-Ordóñez M, Martínez MC (2011) About the role of CK2 in plant signal transduction. Mol Cell Biochem 356:233–240. https://doi.org/10.1007/s11010-011-0970-7
Mu Q, Huang Z, Chakrabarti M, Illa-Berenguer E, Liu X, Wang Y, Ramos A, van der Knaap E (2017) Fruit weight is controlled by cell size regulator encoding a novel protein that is expressed in maturing tomato fruits. PLoS Genet 13:e1006930. https://doi.org/10.1371/journal.pgen.1006930
Mulekar JJ, Huq E (2014) Expanding roles of protein kinase CK2 in regulating plant growth and development. J Exp Bot 65:2883–2893. https://doi.org/10.1093/jxb/ert401
Mulekar JJ, Huq E (2015) Arabidopsis casein kinase 2 α4 subunit regulates various developmental pathways in a functionally overlapping manner. Plant Sci 236:295–303. https://doi.org/10.1016/j.plantsci.2015.04.013
Mulekar JJ, Bu Q, Chen F, Huq E (2012) Casein kinase II α subunits affect multiple developmental and stress-responsive pathways in Arabidopsis. Plant J 69:343–354. https://doi.org/10.1111/j.1365-313X.2011.04794.x
Muños S, Ranc N, Botton E, Bérard A, Rolland S, Duffé P, Carretero Y, Le Paslier M-C, Delalande C, Bouzayen M, Brunel D, Causse M (2011) Increase in tomato locule number is controlled by two single-nucleotide polymorphisms located near WUSCHEL. Plant Physiol 156:2244–2254. https://doi.org/10.1104/pp.111.173997
Negin B, Shemer O, Sorek Y, Eshed Williams L (2017) Shoot stem cell specification in roots by the WUSCHEL transcription factor. PLoS ONE 12:e0176093. https://doi.org/10.1371/journal.pone.0176093
Nguyen HP, Chakravarthy S, Velásquez AC, McLane HL, Zeng L, Nakayashiki H, Park D-H, Collmer A, Martin GB (2010) Methods to study PAMP-triggered immunity using tomato and Nicotiana benthamiana. Mol Plant Microbe Interact 23:991–999. https://doi.org/10.1094/MPMI-23-8-0991
Ogiso E, Takahashi Y, Sasaki T, Yano M, Izawa T (2010) The role of casein kinase II in flowering time regulation has diversified during evolution. Plant Physiol 152:808–820. https://doi.org/10.1104/pp.109.148908
Pazhouhandeh M, Molinier J, Berr A, Genschik P (2011) MSI4/FVE interacts with CUL4-DDB1 and a PRC2-like complex to control epigenetic regulation of flowering time in Arabidopsis. Proc Natl Acad Sci USA 108:3430–3435. https://doi.org/10.1073/pnas.1018242108
Portolés S, Más P (2010) The functional interplay between protein kinase CK2 and CCA1 transcriptional activity is essential for clock temperature compensation in Arabidopsis. PLoS Genet 6:e1001201. https://doi.org/10.1371/journal.pgen.1001201
Rodríguez GR, Muños S, Anderson C, Sim S-C, Michel A, Causse M, Gardener BBM, Francis D, van der Knaap E (2011) Distribution of SUN, OVATE, LC, and FAS in the tomato germplasm and the relationship to fruit shape diversity. Plant Physiol 156:275–285. https://doi.org/10.1104/pp.110.167577
Rodriguez-Leal D, Xu C, Kwon C-T, Soyars C, Demesa-Arevalo E, Man J, Liu L, Lemmon ZH, Jones DS, van Eck J, Jackson DP, Bartlett ME, Nimchuk ZL, Lippman ZB (2019) Evolution of buffering in a genetic circuit controlling plant stem cell proliferation. Nat Genet 51:786–792. https://doi.org/10.1038/s41588-019-0389-8
Russo GL, van den Bos C, Sutton A, Coccetti P, Baroni MD, Alberghina L, Marshak DR (2000) Phosphorylation of Cdc28 and regulation of cell size by the protein kinase CKII in Saccharomyces cerevisiae. Biochem J 351:143–150. https://doi.org/10.1042/0264-6021:3510143
Sablowski R, Carnier Dornelas M (2014) Interplay between cell growth and cell cycle in plants. J Exp Bot 65:2703–2714. https://doi.org/10.1093/jxb/ert354
Sanagi M, Aoyama S, Kubo A, Lu Y, Sato Y, Ito S, Abe M, Mitsuda N, Ohme-Takagi M, Kiba T, Nakagami H, Rolland F, Yamaguchi J, Imaizumi T, Sato T (2021) Low nitrogen conditions accelerate flowering by modulating the phosphorylation state of FLOWERING BHLH 4 in Arabidopsis. Proc Natl Acad Sci USA 118(19):e20229421. https://doi.org/10.1073/pnas.2022942118
Sang Y, Yan F, Ren X (2015) The role and mechanism of CRL4 E3 ubiquitin ligase in cancer and its potential therapy implications. Oncotarget 6:42590–42602. https://doi.org/10.18632/oncotarget.6052
Schoof H, Lenhard M, Haecker A, Mayer KFX, Jürgens G, Laux T (2000) The stem cell population of Arabidopsis shoot meristems is maintained by a regulatory loop between the CLAVATA and WUSCHEL genes. Cell 100:635–644. https://doi.org/10.1016/s0092-8674(00)80700-x
Seo K-I, Lee J-H, Nezames CD, Zhong S, Song E, Byun M-O, Deng XW (2014) ABD1 is an Arabidopsis DCAF substrate receptor for CUL4-DDB1-based E3 ligases that acts as a negative regulator of abscisic acid signaling. Plant Cell 26:695–711. https://doi.org/10.1105/tpc.113.119974
Shimotohno A, Ohno R, Bisova K, Sakaguchi N, Huang J, Koncz C, Uchimiya H, Umeda M (2006) Diverse phosphoregulatory mechanisms controlling cyclin-dependent kinase-activating kinases in Arabidopsis. Plant J 47:701–710. https://doi.org/10.1111/j.1365-313X.2006.02820.x
Sicard A, Petit J, Mouras A, Chevalier C, Hernould M (2008) Meristem activity during flower and ovule development in tomato is controlled by the mini zinc finger gene INHIBITOR OF MERISTEM ACTIVITY. Plant J 55:415–427. https://doi.org/10.1111/j.1365-313X.2008.03520.x
Somssich M, Je BI, Simon R, Jackson D (2016) CLAVATA-WUSCHEL signaling in the shoot meristem. Development 143:3238–3248. https://doi.org/10.1242/dev.133645
St-Denis NA, Litchfield DW (2009) Protein kinase CK2 in health and disease: from birth to death: the role of protein kinase CK2 in the regulation of cell proliferation and survival. Cell Mol Life Sci 66:1817–1829. https://doi.org/10.1007/s00018-009-9150-2
Sun L, Rodriguez GR, Clevenger JP, Illa-Berenguer E, Lin J, Blakeslee JJ, Liu W, Fei Z, Wijeratne A, Meulia T, van der Knaap E (2015) Candidate gene selection and detailed morphological evaluations of fs8.1, a quantitative trait locus controlling tomato fruit shape. J Exp Bot 66:6471–6482. https://doi.org/10.1093/jxb/erv361
Tang X, Liu J, Huang S, Shi W, Miao M, Tang DF, Niu X, Xiao F, Liu Y (2012) Roles of UV-damaged DNA binding protein 1 (DDB1) in epigenetically modifying multiple traits of agronomic importance in tomato. Plant Signal Behav 7:1529–1532. https://doi.org/10.4161/psb.22249
Tang X, Tang Z, Huang S, Liu J, Liu J, Shi W, Tian X, Li Y, Zhang D, Yang J, Gao Y, Zeng D, Hou P, Niu X, Cao Y, Li G, Li X, Xiao F, Liu Y (2013) Whole transcriptome sequencing reveals genes involved in plastid/chloroplast division and development are regulated by the HP1/DDB1 at an early stage of tomato fruit development. Planta 238:923–936. https://doi.org/10.1007/s00425-013-1942-9
Tang X, Miao M, Niu X, Zhang D, Cao X, Jin X, Zhu Y, Fan Y, Wang H, Liu Y, Sui Y, Wang W, Wang A, Xiao F, Giovannoni J, Liu Y (2016) Ubiquitin-conjugated degradation of golden 2-like transcription factor is mediated by CUL4-DDB1-based E3 ligase complex in tomato. New Phytol 209:1028–1039. https://doi.org/10.1111/nph.13635
Wang S, Liu J, Feng Y, Niu X, Giovannoni J, Liu Y (2008) Altered plastid levels and potential for improved fruit nutrient content by downregulation of the tomato DDB1-interacting protein CUL4. Plant J 55:89–103. https://doi.org/10.1111/j.1365-313X.2008.03489.x
Wang F, Zhu D, Huang X, Li S, Gong Y, Yao Q, Fu X, Fan LM, Deng XW (2009) Biochemical insights on degradation of Arabidopsis DELLA proteins gained from a cell-free assay system. Plant Cell 21:2378–2390. https://doi.org/10.1105/tpc.108.065433
Wang F, Deng M, Chen J, He Q, Jia X, Guo H, Xu J, Liu Y, Zhang S, Shou H, Mao C (2020) CASEIN KINASE2-dependent phosphorylation of PHOSPHATE2 fine-tunes phosphate homeostasis in rice. Plant Physiol 183:250–262. https://doi.org/10.1104/pp.20.00078
Wang X, Aguirre L, Rodríguez-Leal D, Hendelman A, Benoit M, Lippman ZB (2021) Dissecting cis-regulatory control of quantitative trait variation in a plant stem cell circuit. Nat Plants 7:419–427. https://doi.org/10.1038/s41477-021-00898-x
Wu S, Xiao H, Cabrera A, Meulia T, van der Knaap E (2011) SUN regulates vegetative and reproductive organ shape by changing cell division patterns. Plant Physiol 157:1175–1186. https://doi.org/10.1104/pp.111.181065
Wu S, Clevenger JP, Sun L, Visa S, Kamiya Y, Jikumaru Y, Blakeslee J, van der Knaap E (2015) The control of tomato fruit elongation orchestrated by sun, ovate and fs8.1 in a wild relative of tomato. Plant Sci 238:95–104. https://doi.org/10.1016/j.plantsci.2015.05.019
Xiao F, Giavalisco P, Martin GB (2007) Pseudomonas syringae type III effector AvrPtoB is phosphorylated in plant cells on serine 258, promoting its virulence activity. J Biol Chem 282:30737–30744. https://doi.org/10.1074/jbc.M705565200
Xing HL, Dong L, Wang ZP, Zhang HY, Han CY, Liu B, Wang XC, Chen QJ (2014) A CRISPR/Cas9 toolkit for multiplex genome editing in plants. BMC Plant Biol 14:327. https://doi.org/10.1186/s12870-014-0327-y
Xu C, Liberatore KL, MacAlister CA, Huang Z, Chu YH, Jiang K, Brooks C, Ogawa-Ohnishi M, Xiong G, Pauly M, van Eck J, Matsubayashi Y, van der Knaap E, Lippman ZB (2015) A cascade of arabinosyltransferases controls shoot meristem size in tomato. Nat Genet 47:784–792. https://doi.org/10.1038/ng.3309
Yang C, Sofroni K, Wijnker E, Hamamura Y, Carstens L, Harashima H, Stolze SC, Vezon D, Chelysheva L, Orban-Nemeth Z, Pochon G, Nakagami H, Schlögelhofer P, Grelon M, Schnittger A (2020) The Arabidopsis Cdk1/Cdk2 homolog CDKA;1 controls chromosome axis assembly during plant meiosis. EMBO J 39:e101625. https://doi.org/10.15252/embj.2019101625
Ying M, Shao X, Jing H, Liu Y, Qi X, Cao J, Chen Y, Xiang S, Song H, Hu R, Wei G, Yang B, He Q (2018) Ubiquitin-dependent degradation of CDK2 drives the therapeutic differentiation of AML by targeting PRDX2. Blood 131:2698–2711. https://doi.org/10.1182/blood-2017-10-813139
Yuste-Lisbona FJ, Fernández-Lozano A, Pineda B, Bretones S, Ortíz-Atienza A, García-Sogo B, Müller NA, Angosto T, Capel J, Moreno V, Jiménez-Gómez JM, Lozano R (2020) ENO regulates tomato fruit size through the floral meristem development network. Proc Natl Acad Sci USA 117:8187–8195. https://doi.org/10.1073/pnas.1913688117
Zhang D, Wang X, Wang M, Li J, Guo X, Chong K, Xu Y (2013) Ectopic expression of WUS in hypocotyl promotes cell division via GRP23 in Arabidopsis. PLoS ONE 8:e75773. https://doi.org/10.1371/journal.pone.0075773
Zhang H, Zhao Y, Zhu JK (2020a) Thriving under stress: how plants balance growth and the stress response. Dev Cell 55:529–543. https://doi.org/10.1016/j.devcel.2020.10.012
Zhang L, Li Z, Garraway J, Cai Q, Zhou Y, Li X, Hu Z, Zhang M, Yang J (2020b) The casein kinase 2 β subunit CK2B1 is required for swollen stem formation via cell cycle control in vegetable Brassica juncea. Plant J 104:706–717. https://doi.org/10.1111/tpj.14958
Zhang H, Zhu J, Gong Z, Zhu JK (2022) Abiotic stress responses in plants. Nat Rev Genet 23:104–119. https://doi.org/10.1038/s41576-021-00413-0
Zhu Y, Huang S, Miao M, Tang X, Yue J, Wang W, Liu Y (2015) Genome-wide identification, sequence characterization, and protein-protein interaction properties of DDB1 (damaged DNA binding protein-1)-binding WD40-repeat family members in Solanum lycopersicum. Planta 241:1337–1350. https://doi.org/10.1007/s00425-015-2258-8
Acknowledgements
This study was supported by grants from the National Natural Science Foundation of China (grant Nos. 31972474, 31671259, 31701922, 31171179, 30825030 and 90717110).
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
Conflict of interest
The authors declare no conflict of interest.
Additional information
Communicated by Dorothea Bartels.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Wang, H., Tang, X. & Liu, Y. SlCK2α as a novel substrate for CRL4 E3 ligase regulates fruit size through maintenance of cell division homeostasis in tomato. Planta 257, 38 (2023). https://doi.org/10.1007/s00425-023-04070-x
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00425-023-04070-x