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Abstract

The anaphase-promoting complex/cyclosome (APC/C) represents a large multisubunit E3-ubiquitin ligase complex that controls the unidirectional progression through the cell cycle by the ubiquitination of specific target proteins, marking them for proteasomal destruction. Although the APC/C's role is largely conserved among eukaryotes, its subunit composition and target spectrum appear to be species specific. In this review, we focus on the plant APC/C complex, whose activity correlates with different developmental processes, including polyploidization and gametogenesis. After an introduction into proteolytic control by ubiquitination, we discuss the composition of the plant APC/C and the essential nature of its core subunits for plant development. Subsequently, we describe the APC/C activator subunits and interactors, most being plant specific. Finally, we provide a comprehensive list of confirmed and suspected plant APC/C target proteins. Identification of growth-related targets might offer opportunities to increase crop yield and resilience of plants to climate change by manipulating APC/C activity.

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2022-10-06
2024-04-19
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Literature Cited

  1. Baloban M, Vanstraelen M, Tarayre S, Reuzeau C, Cultrone A et al. 2013. Complementary and dose-dependent action of AtCCS52A isoforms in endoreduplication and plant size control. New Phytol 198:1049–59
    [Google Scholar]
  2. Blilou I, Frugier F, Folmer S, Serralbo O, Willemsen V et al. 2002. The Arabidopsis HOBBIT gene encodes a CDC27 homolog that links the plant cell cycle to progression of cell differentiation. Genes Dev 16:2566–75
    [Google Scholar]
  3. Boruc J, Van den Daele H, Hollunder J, Rombauts S, Mylle E et al. 2010. Functional modules in the Arabidopsis core cell cycle binary protein–protein interaction network. Plant Cell 22:1264–80
    [Google Scholar]
  4. Boudolf V, Lammens T, Boruc J, Van Leene J, Van den Daele H et al. 2009. CDKB1;1 forms a functional complex with CYCA2;3 to suppress endocycle onset. Plant Physiol 150:1482–93
    [Google Scholar]
  5. Breuer C, Morohashi K, Kawamura A, Takahashi N, Ishida T et al. 2012. Transcriptional repression of the APC/C activator CCS52A1 promotes active termination of cell growth. EMBO J 31:4488–501
    [Google Scholar]
  6. Bulankova P, Riehs-Kearnan N, Nowack MK, Schnittger A, Riha K. 2010. Meiotic progression in Arabidopsis is governed by complex regulatory interactions between SMG7, TDM1, and the meiosis I-specific cyclin TAM. Plant Cell 22:3791–803
    [Google Scholar]
  7. Capron A, Ökrész L, Genschik P. 2003a. First glance at the plant APC/C, a highly conserved ubiquitin–protein ligase. Trends Plant Sci 8:83–89
    [Google Scholar]
  8. Capron A, Serralbo O, Fülöp K, Frugier F, Parmentier Y et al. 2003b. The Arabidopsis anaphase-promoting complex or cyclosome: molecular and genetic characterization of the APC2 subunit. Plant Cell 15:2370–82
    [Google Scholar]
  9. Cebolla A, Vinardell JM, Kiss E, Oláh B, Roudier F et al. 1999. The mitotic inhibitor ccs52 is required for endoreduplication and ploidy-dependent cell enlargement in plants. EMBO J 18:4476–84
    [Google Scholar]
  10. Chen L, Hellmann H. 2013. Plant E3 ligases: flexible enzymes in a sessile world. Mol. Plant 6:1388–404
    [Google Scholar]
  11. Cifuentes M, Jolivet S, Cromer L, Harashima H, Bulankova P et al. 2016. TDM1 regulation determines the number of meiotic divisions. PLOS Genet 12:e1005856
    [Google Scholar]
  12. Cromer L, Heyman J, Touati S, Harashima H, Araou E et al. 2012. OSD1 promotes meiotic progression via APC/C inhibition and forms a regulatory network with TDM and CYCA1;2/TAM. PLOS Genet 8:e1002865
    [Google Scholar]
  13. Cromer L, Jolivet S, Horlow C, Chelysheva L, Heyman J et al. 2013. Centromeric cohesion is protected twice at meiosis, by SHUGOSHINs at anaphase I and by PATRONUS at interkinesis. Curr. Biol. 23:2090–99
    [Google Scholar]
  14. Cromer L, Jolivet S, Singh DK, Berthier F, De Winne N et al. 2019. Patronus is the elusive plant securin, preventing chromosome separation by antagonizing separase. PNAS 116:16018–27
    [Google Scholar]
  15. d'Erfurth I, Cromer L, Jolivet S, Girard C, Horlow C et al. 2010. The CYCLIN-A CYCA1;2/TAM is required for the meiosis I to meiosis II transition and cooperates with OSD1 for the prophase to first meiotic division transition. PLOS Genet 6:e1000989
    [Google Scholar]
  16. d'Erfurth I, Jolivet S, Froger N, Catrice O, Novatchkova M, Mercier R 2009. Turning meiosis into mitosis. PLOS Biol 7:e1000124
    [Google Scholar]
  17. da Fonseca PCA, Kong EH, Zhang Z, Schreiber A, Williams MA et al. 2011. Structures of APC/CCdh1 with substrates identify Cdh1 and Apc10 as the D-box co-receptor. Nature 470:274–48
    [Google Scholar]
  18. Davey NE, Morgan DO. 2016. Building a regulatory network with short linear sequence motifs: lessons from the degrons of the anaphase-promoting complex. Mol. Cell 64:12–23
    [Google Scholar]
  19. Decaestecker W, Buono RA, Pfeiffer ML, Vangheluwe N, Jourquin J et al. 2019. CRISPR-TSKO: a technique for efficient mutagenesis in specific cell types, tissues, or organs in Arabidopsis. Plant Cell 31:2868–87
    [Google Scholar]
  20. Di Fiore B, Davey NE, Hagting A, Izawa D, Mansfeld J et al. 2015. The ABBA motif binds APC/C activators and is shared by APC/C substrates and regulators. Dev. Cell 32:358–72
    [Google Scholar]
  21. Di Fiore B, Pines J. 2007. Emi1 is needed to couple DNA replication with mitosis but does not regulate activation of the mitotic APC/C. J. Cell Biol. 177:425–37
    [Google Scholar]
  22. Eloy N, de Freitas Lima M, Ferreira PCG, Inzé D. 2015. The role of the anaphase-promoting complex/cyclosome in plant growth. Crit. Rev. Plant Sci. 34:487–505
    [Google Scholar]
  23. Eloy NB, de Freitas Lima M, Van Damme D, Vanhaeren H, Gonzalez N et al. 2011. The APC/C subunit 10 plays an essential role in cell proliferation during leaf development. Plant J 68:351–63
    [Google Scholar]
  24. Eloy NB, Gonzalez N, Van Leene J, Maleux K, Vanhaeren H et al. 2012. SAMBA, a plant-specific anaphase-promoting complex/cyclosome regulator is involved in early development and A-type cyclin stabilization. PNAS 109:13853–58
    [Google Scholar]
  25. Eme L, Trilles A, Moreira D, Brochier-Armanet C. 2011. The phylogenomic analysis of the anaphase promoting complex and its targets points to complex and modern-like control of the cell cycle in the last common ancestor of eukaryotes. BMC Evol. Biol. 11:265
    [Google Scholar]
  26. Fülöp K, Tarayre S, Kelemen Z, Horváth G, Kevei Z et al. 2005. Arabidopsis anaphase-promoting complexes: multiple activators and wide range of substrates might keep APC perpetually busy. Cell Cycle 4:1084–92
    [Google Scholar]
  27. Ge L, Chen H, Jiang J-F, Zhao Y, Xu M-L et al. 2004. Overexpression of OsRAA1 causes pleiotropic phenotypes in transgenic rice plants, including altered leaf, flower, and root development and root response to gravity. Plant Physiol 135:1502–13
    [Google Scholar]
  28. Glickman MH, Ciechanover A. 2002. The ubiquitin-proteasome proteolytic pathway: destruction for the sake of construction. Physiol. Rev. 82:373–428
    [Google Scholar]
  29. Glover J, Grelon M, Craig S, Chaudhury A, Dennis E 1998. Cloning and characterization of MS5 from Arabidopsis: a gene critical in male meiosis. Plant J 15:345–56
    [Google Scholar]
  30. Gong P, Bontinck M, Demuynck K, De Block J, Gevaert K et al. 2022. SAMBA controls cell division rate during maize development. Plant Physiol 188:411–24
    [Google Scholar]
  31. Gu F, Bringmann M, Combs JR, Yang J, Bergmann DC, Nielsen E. 2016. Arabidopsis CSLD5 functions in cell plate formation in a cell cycle-dependent manner. Plant Cell 28:1722–37
    [Google Scholar]
  32. Guo L, Jiang L, Lu X-L, Liu C-M. 2018. ANAPHASE PROMOTING COMPLEX/CYCLOSOME-mediated cyclin B1 degradation is critical for cell cycle synchronization in syncytial endosperms. J. Integr. Plant Biol. 60:448–54
    [Google Scholar]
  33. Guo L, Jiang L, Zhang Y, Lu X-L, Xie Q et al. 2016. The anaphase-promoting complex initiates zygote division in Arabidopsis through degradation of cyclin B1. Plant J 86:161–74
    [Google Scholar]
  34. Han Y, Cao H, Jiang J, Xu Y, Du J et al. 2008. Rice ROOT ARCHITECTURE ASSOCIATED1 binds the proteasome subunit RPT4 and is degraded in a D-box and proteasome-dependent manner. Plant Physiol 148:843–55
    [Google Scholar]
  35. Hase Y, Trung KH, Matsunaga T, Tanaka A. 2006. A mutation in the uvi4 gene promotes progression of endo-reduplication and confers increased tolerance towards ultraviolet B light. Plant J 46:317–26
    [Google Scholar]
  36. Hershko A, Ciechanover A. 1998. The ubiquitin system. Annu. Rev. Biochem. 67:425–79
    [Google Scholar]
  37. Heyman J, Cools T, Vandenbussche F, Heyndrickx KS, Van Leene J et al. 2013. ERF115 controls root quiescent center cell division and stem cell replenishment. Science 342:860–63
    [Google Scholar]
  38. Heyman J, De Veylder L. 2012. The anaphase-promoting complex/cyclosome in control of plant development. Mol. Plant 5:1182–94
    [Google Scholar]
  39. Heyman J, Polyn S, Eekhout T, De Veylder L. 2017. Tissue-specific control of the endocycle by the Anaphase Promoting Complex/Cyclosome inhibitors UVI4 and DEL1. Plant Physiol 175:303–13
    [Google Scholar]
  40. Heyman J, Van den Daele H, De Wit K, Boudolf V, Berckmans B et al. 2011. Arabidopsis ULTRAVIOLET-B-INSENSITIVE4 maintains cell division activity by temporal inhibition of the anaphase-promoting complex/cyclosome. Plant Cell 23:4394–410
    [Google Scholar]
  41. Holt LJ, Krutchinsky AN, Morgan DO. 2008. Positive feedback sharpens the anaphase switch. Nature 454:353–57
    [Google Scholar]
  42. Imai KK, Ohashi Y, Tsuge T, Yoshizumi T, Matsui M et al. 2006. The A-type cyclin CYCA2;3 is a key regulator of ploidy levels in Arabidopsis endoreduplication. Plant Cell 18:382–96
    [Google Scholar]
  43. Iwata E, Ikeda S, Matsunaga S, Kurata M, Yoshioka Y et al. 2011. GIGAS CELL1, a novel negative regulator of the anaphase-promoting complex/cyclosome, is required for proper mitotic progression and cell fate determination in Arabidopsis. Plant Cell 23:4382–93
    [Google Scholar]
  44. Izawa D, Pines J. 2015. The mitotic checkpoint complex binds a second CDC20 to inhibit active APC/C. Nature 517:631–34
    [Google Scholar]
  45. Jonak K, Zagoriy I, Oz T, Graf P, Rojas J et al. 2017. APC/C-Cdc20 mediates deprotection of centromeric cohesin at meiosis II in yeast. Cell Cycle 16:1145–52
    [Google Scholar]
  46. Juraniec M, Heyman J, Schubert V, Salis P, De Veylder L, Verbruggen N. 2016. Arabidopsis COPPER MODIFIED RESISTANCE1/PATRONUS1 is essential for growth adaptation to stress and required for mitotic onset control. New Phytol 209:177–91
    [Google Scholar]
  47. Kasili R, Walker JD, Simmons LA, Zhou J, De Veylder L, Larkin JC. 2010. SIAMESE cooperates with the CDH1-like protein CCS52A1 to establish endoreplication in Arabidopsis thaliana trichomes. Genetics 185:257–68
    [Google Scholar]
  48. Kevei Z, Baloban M, Da Ines O, Tiricz H, Kroll A et al. 2011. Conserved CDC20 cell cycle functions are carried out by two of the five isoforms in Arabidopsis thaliana. PLOS ONE 6:e20618
    [Google Scholar]
  49. Kraft C, Vodermaier HC, Maurer-Stroh S, Eisenhaber F, Peters JM. 2005. The WD40 propeller domain of Cdh1 functions as a destruction box receptor for APC/C substrates. Mol. Cell 18:543–53
    [Google Scholar]
  50. Kwee H-S, Sundaresan V. 2003. The NOMEGA gene required for female gametophyte development encodes the putative APC6/CDC16 component of the Anaphase Promoting Complex in Arabidopsis. Plant J 36:853–66
    [Google Scholar]
  51. Lammens T, Boudolf V, Kheibarshekan L, Zalmas LP, Gaamouche T et al. 2008. Atypical E2F activity restrains APC/CCCS52A2 function obligatory for endocycle onset. PNAS 105:14721–26
    [Google Scholar]
  52. Larson-Rabin Z, Li Z, Masson PH, Day CD. 2009. FZR2/CCS52A1 expression is a determinant of endoreduplication and cell expansion in Arabidopsis. Plant Physiol 149:874–84
    [Google Scholar]
  53. Li Z, Zhang D, Xiong X, Yan B, Xie W et al. 2017. A potent Cas9-derived gene activator for plant and mammalian cells. Nat. Plants 3:930–36
    [Google Scholar]
  54. Lin Q, Wang D, Dong H, Gu S, Cheng Z et al. 2012. Rice APC/CTE controls tillering by mediating the degradation of MONOCULM 1. Nat. Commun. 3:752
    [Google Scholar]
  55. Lin Q, Wu F, Sheng P, Zhang Z, Zhang X et al. 2015. The SnRK2-APC/CTE regulatory module mediates the antagonistic action of gibberellic acid and abscisic acid pathways. Nat. Commun. 6:7981
    [Google Scholar]
  56. Lin Q, Zhang Z, Wu F, Feng M, Sun Y et al. 2020. The APC/CTE E3 ubiquitin ligase complex mediates the antagonistic regulation of root growth and tillering by ABA and GA. Plant Cell 32:1973–87
    [Google Scholar]
  57. Lin Y-N, Jiang C-K, Cheng Z-K, Wang D-H, Shen L-P et al. 2022. Rice Cell Division Cycle 20s are required for faithful chromosome segregation and cytokinesis during meiosis. Plant Physiol. 188:1111–28
    [Google Scholar]
  58. Liu Y, Ye W, Li B, Zhou X, Cui Y et al. 2012. CCS52A2/FZR1, a cell cycle regulator, is an essential factor for shoot apical meristem maintenance in Arabidopsis thaliana. BMC Plant Biol 12:135
    [Google Scholar]
  59. Liu Z, Chen G, Gao F, Xu R, Li N et al. 2019. Transcriptional repression of the APC/C activator genes CCS52A1/A2 by the mediator complex subunit MED16 controls endoreduplication and cell growth in Arabidopsis. Plant Cell 31:1899–912
    [Google Scholar]
  60. Lorenzo-Orts L, Witthoeft J, Deforges J, Martinez J, Loubéry S et al. 2019. Concerted expression of a cell cycle regulator and a metabolic enzyme from a bicistronic transcript in plants. Nat. Plants 5:184–93
    [Google Scholar]
  61. Lowder LG, Zhou J, Zhang Y, Malzahn A, Zhong Z et al. 2018. Robust transcriptional activation in plants using multiplexed CRISPR-Act2.0 and mTALE-Act systems. Mol. Plant 11:245–56
    [Google Scholar]
  62. Magyar Z, Horváth B, Khan S, Mohammed B, Henriques R et al. 2012. Arabidopsis E2FA stimulates proliferation and endocycle separately through RBR-bound and RBR-free complexes. EMBO J 31:1480–93
    [Google Scholar]
  63. Mansfeld J, Collin P, Collins MO, Choudhary JS, Pines J 2011. APC15 drives the turnover of MCC-CDC20 to make the spindle assembly checkpoint responsive to kinetochore attachment. Nat. Cell Biol. 13:1234–43
    [Google Scholar]
  64. Marrocco K, Bergdoll M, Achard P, Criqui M-C, Genschik P. 2010. Selective proteolysis sets the tempo of the cell cycle. Curr. Opin. Plant Biol. 13:631–39
    [Google Scholar]
  65. Marrocco K, Criqui M-C, Zervudacki J, Schott G, Eisler H et al. 2012. APC/C-mediated degradation of dsRNA-binding protein 4 (DRB4) involved in RNA silencing. PLOS ONE 7:e35173
    [Google Scholar]
  66. Marrocco K, Thomann A, Parmentier Y, Genschik P, Criqui M-C. 2009. The APC/C E3 ligase remains active in most post-mitotic Arabidopsis cells and is required for proper vasculature development and organization. Development 136:1475–85
    [Google Scholar]
  67. Mathieu-Rivet E, Gévaudant F, Sicard A, Salar S, Do PT et al. 2010. Functional analysis of the anaphase promoting complex activator CCS52A highlights the crucial role of endo-reduplication for fruit growth in tomato. Plant J 62:727–41
    [Google Scholar]
  68. Moradpour M, Abdulah SNA. 2020. CRISPR/dCas9 platforms in plants: strategies and applications beyond genome editing. Plant Biotechnol. J. 18:32–44
    [Google Scholar]
  69. Morgan DO. 2007. The Cell Cycle: Principles of Control London: New Science
  70. Niu B, Wang L, Zhang L, Ren D, Ren R et al. 2015. Arabidopsis Cell Division Cycle 20.1 is required for normal meiotic spindle assembly and chromosome segregation. Plant Cell 27:3367–82
    [Google Scholar]
  71. Ogawa D, Abe K, Miyao A, Kojima M, Sakakibara H et al. 2011. RSS1 regulates the cell cycle and maintains meristematic activity under stress conditions in rice. Nat. Commun. 2:278
    [Google Scholar]
  72. Ohe M, Inoue D, Kanemori Y, Sagata N. 2007. Erp1/Emi2 is essential for the meiosis I to meiosis II transition in Xenopus oocytes. Dev. Biol. 303:157–64
    [Google Scholar]
  73. Perazza D, Herzog M, Hülskamp M, Brown S, Dorne A-M, Bonneville J-M. 1999. Trichome cell growth in Arabidopsis thaliana can be derepressed by mutations in at least five genes. Genetics 152:461–76
    [Google Scholar]
  74. Pérez-Pérez JM, Serralbo O, Vanstraelen M, González C, Criqui M-C et al. 2008. Specialization of CDC27 function in the Arabidopsis thaliana anaphase-promoting complex (APC/C). Plant J 53:78–89
    [Google Scholar]
  75. Peters J-M. 2002. The anaphase-promoting complex: proteolysis in mitosis and beyond. Mol. Cell 9:931–43
    [Google Scholar]
  76. Pfeiffer ML, Winkler J, Van Damme D, Jacobs TB, Nowack MK. 2021. Conditional and tissue-specific approaches to dissect essential mechanisms in plant development. Curr. Opin. Plant Biol. 65:102119
    [Google Scholar]
  77. Pfleger CM, Kirschner MW. 2000. The KEN box: an APC recognition signal distinct from the D box targeted by Cdh1. Genes Dev 14:655–65
    [Google Scholar]
  78. Qin L, Guimarães DSPSF, Melesse M, Hall MC. 2016. Substrate recognition by the Cdh1 destruction box receptor is a general requirement for APC/CCdh1-mediated proteolysis. J. Biol. Chem. 291:15564–74
    [Google Scholar]
  79. Rojas CA, Eloy NB, de Freitas Lima M, Rodrigues RL, Ozório Franco L et al. 2009. Overexpression of the Arabidopsis anaphase promoting complex subunit CDC27a increases growth rate and organ size. Plant Mol. Biol. 71:307–18
    [Google Scholar]
  80. Ross KJ, Fransz P, Armstrong SJ, Vizir I, Mulligan B et al. 1997. Cytological characterization of four meiotic mutants of Arabidopsis isolated from T-DNA-transformed lines. Chromosome Res 5:551–59
    [Google Scholar]
  81. Saze H, Kakutani T. 2007. Heritable epigenetic mutation of a transposon-flanked Arabidopsis gene due to lack of the chromatin-remodeling factor DDM1. EMBO J 26:3641–52
    [Google Scholar]
  82. Schnell JD, Hicke L. 2003. Non-traditional functions of ubiquitin and ubiquitin-binding proteins. J. Biol. Chem. 278:35857–60
    [Google Scholar]
  83. Schreiber A, Stengel F, Zhang Z, Enchev RI, Kong EH et al. 2011. Structural basis for the subunit assembly of the anaphase-promoting complex. Nature 470:227–32
    [Google Scholar]
  84. Schrock MS, Stromberg BR, Scarberry L, Summers MK. 2020. APC/C ubiquitin ligase: functions and mechanisms in tumorigenesis. Semin. Cancer Biol 67:80–91
    [Google Scholar]
  85. Schwickart M, Havlis J, Habermann B, Bogdanova A, Camasses A et al. 2004. Swm1/Apc13 is an evolutionarily conserved subunit of the anaphase-promoting complex stabilizing the association of Cdc16 and Cdc27. Mol. Cell. Biol. 24:3562–76
    [Google Scholar]
  86. Serralbo O, Pérez-Pérez JM, Heidstra R, Scheres B. 2006. Non-cell-autonomous rescue of anaphase-promoting complex function revealed by mosaic analysis of HOBBIT, an Arabidopsis CDC27 homolog. PNAS 103:13250–55
    [Google Scholar]
  87. Su'udi M, Cha J-Y, Ahn I-P, Kwak Y-S, Woo Y-M, Son D 2012. Functional characterization of a B-type cell cycle switch 52 in rice (OsCCS52B). Plant Cell Tissue Organ Cult 111:101–11
    [Google Scholar]
  88. Sullivan M, Morgan DO. 2007. Finishing mitosis, one step at a time. Nat. Rev. Mol. Cell Biol. 8:894–903
    [Google Scholar]
  89. Takahashi N, Kajihara T, Okamura C, Kim Y, Katagiri Y et al. 2013. Cytokinins control endocycle onset by promoting the expression of an APC/C activator in Arabidopsis roots. Curr. Biol. 23:1812–17
    [Google Scholar]
  90. Tang Z, Li B, Bharadwaj R, Zhu H, Özkan E et al. 2001. APC2 Cullin protein and APC11 RING protein comprise the minimal ubiquitin ligase module of the anaphase-promoting complex. Mol. Biol. Cell 12:3839–51
    [Google Scholar]
  91. Tarayre S, Vinardell JM, Cebolla A, Kondorosi A, Kondorosi E. 2004. Two classes of the CDh1-type activators of the anaphase-promoting complex in plants: novel functional domains and distinct regulation. Plant Cell 16:422–34
    [Google Scholar]
  92. Thornton BR, Ng TM, Matyskiela ME, Carroll CW, Morgan DO, Toczyski DP. 2006. An architectural map of the anaphase-promoting complex. Genes Dev 20:449–60
    [Google Scholar]
  93. Tung JJ, Hansen DV, Ban KH, Loktev AV, Summers MK et al. 2005. A role for the anaphase-promoting complex inhibitor Emi2/XErp1, a homolog of early mitotic inhibitor 1, in cytostatic factor arrest of Xenopus eggs. PNAS 102:4318–23
    [Google Scholar]
  94. Uzunova K, Dye BT, Schutz H, Ladurner R, Petzold G et al. 2012. APC15 mediates CDC20 autoubiquitylation by APC/CMCC and disassembly of the mitotic checkpoint complex. Nat. Struct. Mol. Biol. 19:1116–23
    [Google Scholar]
  95. Van Leene J, Hollunder J, Eeckhout D, Persiau G, Van De Slijke E et al. 2010. Targeted interactomics reveals a complex core cell cycle machinery in Arabidopsis thaliana. Mol. Syst. Biol. 6:397
    [Google Scholar]
  96. Vandepoele K, Raes J, De Veylder L, Rouzé P, Rombauts S, Inzé D. 2002. Genome-wide analysis of core cell cycle genes in Arabidopsis. Plant Cell 14:903–16
    [Google Scholar]
  97. Vanstraelen M, Baloban M, Da Ines O, Cultrone A, Lammens T et al. 2009. APC/CCCS52A complexes control meristem maintenance in the Arabidopsis root. PNAS 106:11806–11
    [Google Scholar]
  98. Vlieghe K, Boudolf V, Beemster GTS, Maes S, Magyar Z et al. 2005. The DP-E2F-like gene DEL1 controls the endocycle in Arabidopsis thaliana. Curr. Biol. 15:59–63
    [Google Scholar]
  99. Wang M, Tang D, Wang K, Shen Y, Qin B et al. 2011. OsSGO1 maintains synaptonemal complex stabilization in addition to protecting centromeric cohesion during rice meiosis. Plant J 67:583–94
    [Google Scholar]
  100. Wang Y, Hou Y, Gu H, Kang D, Chen Z et al. 2012. The Arabidopsis APC4 subunit of the anaphase-promoting complex/cyclosome (APC/C) is critical for both female gametogenesis and embryogenesis. Plant J 69:227–40
    [Google Scholar]
  101. Wang Y, Hou Y, Gu H, Kang D, Chen Z-L et al. 2013. The Arabidopsis anaphase-promoting complex/cyclosome subunit 1 is critical for both female gametogenesis and embryogenesis J. Integr. Plant Biol. 55:64–74
    [Google Scholar]
  102. Willems A, Heyman J, Eekhout T, Achon I, Pedroza-Garcia JA 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 32:2979–96
    [Google Scholar]
  103. Willemsen V, Wolkenfelt H, de Vrieze G, Weisbeek P, Scheres B. 1998. The HOBBIT gene is required for formation of the root meristem in the Arabidopsis embryo. Development 125:521–31
    [Google Scholar]
  104. Xu C, Wang Y, Yu Y, Duan J, Liao Z et al. 2012. Degradation of MONOCULM 1 by APC/CTAD1 regulates rice tillering. Nat. Commun. 3:750
    [Google Scholar]
  105. Xu R-Y, Xu J, Wang L, Niu B, Copenhaver GP et al. 2019. The Arabidopsis anaphase-promoting complex/cyclosome subunit 8 is required for male meiosis. New Phytol 224:229–41
    [Google Scholar]
  106. Xu Y, Cao H, Chong K 2010. APC-targeted RAA1 degradation mediates the cell cycle and root development in plants. Plant Signal. Behav. 5:218–23
    [Google Scholar]
  107. Xu Y, Jin W, Li N, Zhang W, Liu C et al. 2016. UBIQUITIN-SPECIFIC PROTEASE14 interacts with ULTRAVIOLET-B INSENSITIVE4 to regulate endoreduplication and cell and organ growth in Arabidopsis. Plant Cell 28:1200–14
    [Google Scholar]
  108. Yang W, Wightman R, Meyerowitz EM. 2017. Cell cycle control by nuclear sequestration of CDC20 and CDH1 mRNA in plant stem cells. Mol. Cell 68:1108–19
    [Google Scholar]
  109. Zamariola L, De Storme N, Vannerum K, Vandepoele K, Armstrong SJ et al. 2014. SHUGOSHINs and PATRONUS protect meiotic centromere cohesion in Arabidopsis thaliana. Plant J 77:782–94
    [Google Scholar]
  110. Zheng B, Chen X, McCormick S 2011. The anaphase-promoting complex is a dual integrator that regulates both microRNA-mediated transcriptional regulation of Cyclin B1 and degradation of Cyclin B1 during Arabidopsis male gametophyte development. Plant Cell 23:1033–46
    [Google Scholar]
  111. Zhong S, Xu Y, Yu C, Zhang X, Li L et al. 2019. Anaphase-promoting complex/cyclosome regulates RdDM activity by degrading DMS3 in Arabidopsis. PNAS 116:3899–908
    [Google Scholar]
  112. Zhou Z, He M, Shah AA, Wan Y. 2016. Insights into APC/C: from cellular function to diseases and therapeutics. Cell Div 11:9
    [Google Scholar]
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