1932

Abstract

Developmental and environmental signals converge on cell cycle machinery to achieve proper and flexible organogenesis under changing environments. Studies on the plant cell cycle began 30 years ago, and accumulated research has revealed many links between internal and external factors and the cell cycle. In this review, we focus on how phytohormones and environmental signals regulate the cell cycle to enable plants to cope with a fluctuating environment. After introducing key cell cycle regulators, we first discuss how phytohormones and their synergy are important for regulating cell cycle progression and how environmental factors positively and negatively affect cell division. We then focus on the well-studied example of stress-induced G2 arrest and view the current model from an evolutionary perspective. Finally, we discuss the mechanisms controlling the transition from the mitotic cycle to the endocycle, which greatly contributes to cell enlargement and resultant organ growth in plants.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-arplant-080720-103739
2021-06-17
2024-04-20
Loading full text...

Full text loading...

/deliver/fulltext/arplant/72/1/annurev-arplant-080720-103739.html?itemId=/content/journals/10.1146/annurev-arplant-080720-103739&mimeType=html&fmt=ahah

Literature Cited

  1. 1. 
    Achard P, Gusti A, Cheminant S, Alioua M, Dhondt S et al. 2009. Gibberellin signaling controls cell proliferation rate in Arabidopsis. Curr. Biol. 19:141188–93
    [Google Scholar]
  2. 2. 
    Adachi S, Minamisawa K, Okushima Y, Inagaki S, Yoshiyama K et al. 2011. Programmed induction of endoreduplication by DNA double-strand breaks in Arabidopsis. PNAS 108:2410004–9
    [Google Scholar]
  3. 3. 
    Andersen SU, Buechel S, Zhao Z, Ljung K, Novák O et al. 2008. Requirement of B2-type cyclin-dependent kinases for meristem integrity in Arabidopsis thaliana. Plant Cell 20:188–100
    [Google Scholar]
  4. 4. 
    Attwooll C, Lazzerini Denchi E, Helin K 2004. The E2F family: specific functions and overlapping interests. EMBO J 23:244709–16
    [Google Scholar]
  5. 5. 
    Baerenfaller K, Massonnet C, Walsh S, Baginsky S, Bühlmann P et al. 2012. Systems-based analysis of Arabidopsis leaf growth reveals adaptation to water deficit. Mol. Syst. Biol. 8:606
    [Google Scholar]
  6. 6. 
    Barkla BJ, Rhodes T, Tran KT, Wijesinghege C, Larkin JC, Dassanayake M. 2018. Making epidermal bladder cells bigger: developmental- and salinity-induced endopolyploidy in a model halophyte. Plant Physiol 177:2615–32
    [Google Scholar]
  7. 7. 
    Barzilai A, Yamamoto KI. 2004. DNA damage responses to oxidative stress. DNA Repair 3:8–91109–15
    [Google Scholar]
  8. 8. 
    Beemster GT, De Veylder L, Vercruysse S, West G, Rombaut D et al. 2005. Genome-wide analysis of gene expression profiles associated with cell cycle transitions in growing organs of Arabidopsis. Plant Physiol 138:2734–43
    [Google Scholar]
  9. 9. 
    Beemster GT, Vercruysse S, De Veylder L, Kuiper M, Inzé D. 2006. The Arabidopsis leaf as a model system for investigating the role of cell cycle regulation in organ growth. J. Plant Res. 119:143–50
    [Google Scholar]
  10. 10. 
    Berckmans B, Lammens T, Van Den Daele H, Magyar Z, Bögre L, De Veylder L. 2011. Light-dependent regulation of DEL1 is determined by the antagonistic action of E2Fb and E2Fc. Plant Physiol 157:31440–51
    [Google Scholar]
  11. 11. 
    Bhosale R, Maere S, De Veylder L. 2019. Endoreplication as a potential driver of cell wall modifications. Curr. Opin. Plant Biol. 51:58–65
    [Google Scholar]
  12. 12. 
    Blackford AN, Jackson SP. 2017. ATM, ATR, and DNA-PK: the trinity at the heart of the DNA damage response. Mol. Cell 66:6801–17
    [Google Scholar]
  13. 13. 
    Boniotti MB, Gutierrez C. 2001. A cell-cycle-regulated kinase activity phosphorylates plant retinoblastoma protein and contains, in Arabidopsis, a CDKA/cyclin D complex. Plant J 28:3341–50
    [Google Scholar]
  14. 14. 
    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 22:41264–80
    [Google Scholar]
  15. 15. 
    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 150:31482–93
    [Google Scholar]
  16. 16. 
    Bourbousse C, Vegesna N, Law JA 2018. SOG1 activator and MYB3R repressors regulate a complex DNA damage network in Arabidopsis. PNAS 115:52E12453–62
    [Google Scholar]
  17. 17. 
    Canher B, Heyman J, Savina M, Devendran A, Eekhout T et al. 2020. Rocks in the auxin stream: Wound-induced auxin accumulation and ERF115 expression synergistically drive stem cell regeneration. PNAS 117:2816667–77
    [Google Scholar]
  18. 18. 
    Cebolla A, Vinardell JM, Kiss E, Olah B, Roudier F et al. 1999. The mitotic inhibitor ccs52 is required for endoreduplication and ploidy-dependent cell enlargement in plants. EMBO J 18:164476–84
    [Google Scholar]
  19. 19. 
    Ceccarelli M, Santantonio E, Marmottini F, Amzallag GN, Cionini PG. 2006. Chromosome endoreduplication as a factor of salt adaptation in Sorghum bicolor. Protoplasma 227:2–4113–18
    [Google Scholar]
  20. 20. 
    Chandran D, Inada N, Hather G, Kleindt CK, Wildermuth MC 2010. Laser microdissection of Arabidopsis cells at the powdery mildew infection site reveals site-specific processes and regulators. PNAS 107:1460–65
    [Google Scholar]
  21. 21. 
    Chen P, Takatsuka H, Takahashi N, Kurata R, Fukao Y et al. 2017. Arabidopsis R1R2R3-Myb proteins are essential for inhibiting cell division in response to DNA damage. Nat. Commun 8:1635Identifies the regulatory mechanism underlying Rep-MYB stability and its essential role in DNA damage–induced cell cycle arrest.
    [Google Scholar]
  22. 22. 
    Cheng Z, Sun L, Qi T, Zhang B, Peng W et al. 2011. The bHLH transcription factor MYC3 interacts with the Jasmonate ZIM-domain proteins to mediate jasmonate response in Arabidopsis. Mol. Plant 4:2279–88
    [Google Scholar]
  23. 23. 
    Churchman ML, Brown ML, Kato N, Kirik V, Hülskamp M et al. 2006. SIAMESE, a plant-specific cell cycle regulator, controls endoreplication onset in Arabidopsis thaliana. Plant Cell 18:113145–57
    [Google Scholar]
  24. 24. 
    Costas C, de la Paz Sanchez M, Stroud H, Yu Y, Oliveros JC et al. 2011. Genome-wide mapping of Arabidopsis thaliana origins of DNA replication and their associated epigenetic marks. Nat. Struct. Mol. Biol. 18:3395–400
    [Google Scholar]
  25. 25. 
    Coudreuse D, Nurse P. 2010. Driving the cell cycle with a minimal CDK control network. Nature 468:73271074–79
    [Google Scholar]
  26. 26. 
    Crncec A, Hochegger H. 2019. Triggering mitosis. FEBS Lett 593:202868–88
    [Google Scholar]
  27. 27. 
    Cruz-Ramírez A, Díaz-Triviño S, Blilou I, Grieneisen VA, Sozzani R et al. 2012. A bistable circuit involving SCARECROW-RETINOBLASTOMA integrates cues to inform asymmetric stem cell division. Cell 150:51002–15
    [Google Scholar]
  28. 28. 
    de Almeida Engler J, Kyndt T, Vieira P, Van Cappelle E, Boudolf V et al. 2012. CCS52 and DEL1 genes are key components of the endocycle in nematode-induced feeding sites. Plant J 72:2185–98
    [Google Scholar]
  29. 29. 
    de Jager SM, Scofield S, Huntley RP, Robinson AS, den Boer BGW, Murray JAH. 2009. Dissecting regulatory pathways of G1/S control in Arabidopsis: common and distinct targets of CYCD3;1, E2Fa and E2Fc. Plant Mol. Biol. 71:4–5345–65
    [Google Scholar]
  30. 30. 
    De Schutter K, Joubès J, Cools T, Verkest A, Corellou F et al. 2007. Arabidopsis WEE1 kinase controls cell cycle arrest in response to activation of the DNA integrity checkpoint. Plant Cell 19:1211–25
    [Google Scholar]
  31. 31. 
    De Veylder L, Larkin JC, Schnittger A. 2011. Molecular control and function of endoreplication in development and physiology. Trends Plant Sci 16:11624–34
    [Google Scholar]
  32. 32. 
    Dehghan Nayeri F 2014. Identification of transcription factors linked to cell cycle regulation in Arabidopsis. Plant Signal. Behav. 9:11e972864
    [Google Scholar]
  33. 33. 
    del Pozo JC, Diaz-Trivino S, Cisneros N, Gutierrez C. 2006. The balance between cell division and endoreplication depends on E2FC-DPB, transcription factors regulated by the ubiquitin-SCFSKP2A pathway in Arabidopsis. Plant Cell 18:92224–35
    [Google Scholar]
  34. 34. 
    den Boer BGW, Murray JAH. 2000. Triggering the cell cycle in plants. Trends Cell Biol 10:6245–50
    [Google Scholar]
  35. 35. 
    Desvoyes B, Fernández-Marcos M, Sequeira-Mendes J, Otero S, Vergara Z, Gutierrez C. 2014. Looking at plant cell cycle from the chromatin window. Front. Plant Sci. 5:369
    [Google Scholar]
  36. 36. 
    Dobrenel T, Caldana C, Hanson J, Robaglia C, Vincentz M et al. 2016. TOR signaling and nutrient sensing. Annu. Rev. Plant Biol. 67:261–85
    [Google Scholar]
  37. 37. 
    Duan G-L, Zhou Y, Tong Y-P, Mukhopadhyay R, Rosen BP, Zhu Y-G. 2007. A CDC25 homologue from rice functions as an arsenate reductase. New Phytol 174:2311–21
    [Google Scholar]
  38. 38. 
    Dubois M, Selden K, Bediée A, Rolland G, Baumberger N et al. 2018. SIAMESE-RELATED1 is regulated posttranslationally and participates in repression of leaf growth under moderate drought. Plant Physiol 176:42834–50
    [Google Scholar]
  39. 39. 
    Dyson N. 1998. The regulation of E2F by pRB-family proteins. Genes Dev 12:152245–62
    [Google Scholar]
  40. 40. 
    Engelen-Eigles G, Jones RJ, Phillips RL. 2001. DNA endoreduplication in maize endosperm cells is reduced by high temperature during the mitotic phase. Crop. Sci. 41:41114–21
    [Google Scholar]
  41. 41. 
    Evans T, Rosenthal ET, Youngblom J, Distel D, Hunt T. 1983. Cyclin: a protein specified by maternal mRNA in sea urchin eggs that is destroyed at each cleavage division. Cell 33:2389–96
    [Google Scholar]
  42. 42. 
    Fabian T, Lorbiecke R, Umeda M, Sauter M. 2000. The cell cycle genes cycA1;1 and cdc2Os-3 are coordinately regulated by gibberellin in planta. Planta 211:3376–83
    [Google Scholar]
  43. 43. 
    Fabian-Marwedel T, Umeda M, Sauter M. 2002. The rice cyclin-dependent kinase–activating kinase R2 regulates S-phase progression. Plant Cell 14:1197–210
    [Google Scholar]
  44. 44. 
    Feng G, Burleigh JG, Braun EL, Mei W, Barbazuk WB. 2017. Evolution of the 3R-MYB gene family in plants. Genome Biol. Evol. 9:41013–29
    [Google Scholar]
  45. 45. 
    Ferguson BJ, Mathesius U. 2014. Phytohormone regulation of legume-rhizobia interactions. J. Chem. Ecol. 40:7770–90
    [Google Scholar]
  46. 46. 
    Ferreira PC, Hemerly AS, Villarroel R, Van Montagu M, Inzé D. 1991. The Arabidopsis functional homolog of the p34cdc2 protein kinase. Plant Cell 3:5531–40
    [Google Scholar]
  47. 47. 
    Forsburg SL, Nurse P. 1991. Cell cycle regulation in the yeasts Saccharomyces cerevisiae and Schizosaccharomyces pombe. Annu. Rev. Cell Biol. 7:227–56
    [Google Scholar]
  48. 48. 
    Fu FQ, Mao WH, Shi K, Zhou YH, Asami T, Yu JQ. 2008. A role of brassinosteroids in early fruit development in cucumber. J. Exp. Bot. 59:92299–308
    [Google Scholar]
  49. 49. 
    Galbraith DW, Harkins KR, Knapp S. 1991. Systemic endopolyploidy in Arabidopsis thaliana. Plant Physiol 96:3985–89
    [Google Scholar]
  50. 50. 
    Gendreau E, Traas J, Desnos T, Grandjean O, Caboche M, Höfte H. 1997. Cellular basis of hypocotyl growth in Arabidopsis thaliana. Plant Physiol 114:1295–305
    [Google Scholar]
  51. 51. 
    Georgii E, Kugler K, Pfeifer M, Vanzo E, Block K et al. 2019. The systems architecture of molecular memory in poplar after abiotic stress. Plant Cell 31:2346–67
    [Google Scholar]
  52. 52. 
    González-Barrios R, Soto-Reyes E, Herrera LA. 2012. Assembling pieces of the centromere epigenetics puzzle. Epigenetics 7:13–13
    [Google Scholar]
  53. 53. 
    González-García MP, Vilarrasa-Blasi J, Zhiponova M, Divol F, Mora-García S et al. 2011. Brassinosteroids control meristem size by promoting cell cycle progression in Arabidopsis roots. Development 138:5849–59
    [Google Scholar]
  54. 54. 
    Gutierrez C. 2009. The Arabidopsis cell division cycle.. Arabidopsis Book 7:e0120
    [Google Scholar]
  55. 55. 
    Hacham Y, Holland N, Butterfield C, Ubeda-Tomas S, Bennett MJ et al. 2011. Brassinosteroid perception in the epidermis controls root meristem size. Development 138:5839–48
    [Google Scholar]
  56. 56. 
    Han SK, Qi X, Sugihara K, Dang JH, Endo TA et al. 2018. MUTE directly orchestrates cell-state switch and the single symmetric division to create stomata. Dev. Cell 45:3303–15.e5
    [Google Scholar]
  57. 57. 
    Harashima H, Dissmeyer N, Schnittger A. 2013. Cell cycle control across the eukaryotic kingdom. Trends Cell Biol 23:7345–56
    [Google Scholar]
  58. 58. 
    Hartwell LH, Culotti J, Pringle JR, Reid BJ. 1974. Genetic control of the cell division cycle in yeast. Science 183:412046–51
    [Google Scholar]
  59. 59. 
    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 46:2317–26
    [Google Scholar]
  60. 60. 
    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 342:6160860–63Demonstrates that BR-dependent expression of ERF115 plays a crucial role in QC cell division.
    [Google Scholar]
  61. 61. 
    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 175:1303–13
    [Google Scholar]
  62. 62. 
    Himanen K, Boucheron E, Vanneste S, de Almeida Engler J, Inzé D, Beekman T. 2002. Auxin-mediated cell cycle activation during early lateral root initiation. Plant Cell 14:102339–51
    [Google Scholar]
  63. 63. 
    Himanen K, Vuylsteke M, Vanneste S, Vercruysse S, Boucheron E et al. 2004. Transcript profiling of early lateral root initiation. PNAS 101:145146–51
    [Google Scholar]
  64. 64. 
    Hirayama T, Imajuku Y, Anai T, Matsui M, Oka A. 1991. Identification of two cell-cycle-controlling cdc2 gene homologs in Arabidopsis thaliana. Gene 105:2159–65
    [Google Scholar]
  65. 65. 
    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 18:2382–96
    [Google Scholar]
  66. 66. 
    Inzé D, De Veylder L. 2006. Cell cycle regulation in plant development. Annu. Rev. Genet. 40:77–105
    [Google Scholar]
  67. 67. 
    Jacob Y, Bergamin E, Donoghue MT, Mongeon V, LeBlanc C et al. 2014. Selective methylation of histone H3 variant H3.1 regulates heterochromatin replication. Science 343:61761249–53
    [Google Scholar]
  68. 68. 
    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 185:1257–68
    [Google Scholar]
  69. 69. 
    Kawamura K, Murray JA, Shinmyo A, Sekine M. 2006. Cell cycle regulated D3-type cyclins form active complexes with plant-specific B-type cyclin-dependent kinase in vitro. Plant Mol. Biol. 61:1–2311–27
    [Google Scholar]
  70. 70. 
    Kirik A, Pecinka A, Wendeler E, Reiss B. 2006. The chromatin assembly factor subunit FASCIATA1 is involved in homologous recombination in plants. Plant Cell 18:102431–42
    [Google Scholar]
  71. 71. 
    Kobayashi K, Suzuki T, Iwata E, Nakamichi N, Suzuki T et al. 2015. Transcriptional repression by MYB3R proteins regulates plant organ growth. EMBO J 34:151992–2007Identifies the core components of DREAM/dREAM-like complexes and their ingenious function in the G2/M transition.
    [Google Scholar]
  72. 72. 
    Koch G, Rolland G, Dauzat M, Bédiée A, Baldazzi V et al. 2019. Leaf production and expansion: a generalized response to drought stresses from cells to whole leaf biomass—a case study in the tomato compound leaf. Plants 8:10409
    [Google Scholar]
  73. 73. 
    Koens KB, Nicoloso FT, Harteveld M, Libbenga KR, Kijne JW. 1995. Auxin starvation results in G2 arrest in suspension-cultured tobacco cells. J. Plant Physiol 147:3–4391–96
    [Google Scholar]
  74. 74. 
    Kono A, Umeda-Hara C, Lee J, Ito M, Uchimiya H et al. 2003. Arabidopsis D-type cyclin CYCD4;1 is a novel cyclin partner of B2-type cyclin-dependent kinase. Plant Physiol 132:31315–21
    [Google Scholar]
  75. 75. 
    Koroleva OA, Tomlinson M, Parinyapong P, Sakvarelidze L, Leader D et al. 2004. CycD1, a putative G1 cyclin from Antirrhinum majus, accelerates the cell cycle in cultured tobacco BY-2 cells by enhancing both G1/S entry and progression through S and G2 phases. Plant Cell 16:92364–79
    [Google Scholar]
  76. 76. 
    Kudo N, Mii M. 2004. Endoreduplication cycles during hypocotyl growth of cabbage (Brassica oleracea L.) under light and dark conditions. Plant Biotechnol 21:4295–98
    [Google Scholar]
  77. 77. 
    Kudo T, Terashima S, Takaki Y, Tomita K, Saito M et al. 2017. PlantExpress: a database integrating OryzaExpress and ArthaExpress for single-species and cross-species gene expression network analyses with microarray-based transcriptome data. Plant Cell Physiol 58:1e1
    [Google Scholar]
  78. 78. 
    Kumar N, Harashima H, Kalve S, Bramsiepe J, Wang K et al. 2015. Functional conservation in the SIAMESE-RELATED family of cyclin-dependent kinase inhibitors in land plants. Plant Cell 27:113065–80
    [Google Scholar]
  79. 79. 
    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 105:3814721–26
    [Google Scholar]
  80. 80. 
    Landrieu I, da Costa M, De Veylder L, Dewitte F, Vandepoele K et al. 2004. A small CDC25 dual-specificity tyrosine-phosphatase isoform in Arabidopsis thaliana. PNAS 101:3613380–85
    [Google Scholar]
  81. 81. 
    Lang L, Schnittger A. 2020. Endoreplication—a means to an end in cell growth and stress response. Curr. Opin. Plant Biol. 54:85–92
    [Google Scholar]
  82. 82. 
    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 149:2874–84
    [Google Scholar]
  83. 83. 
    Lavin MF, Gueven N. 2006. The complexity of p53 stabilization and activation. Cell Death Differ 13:941–50
    [Google Scholar]
  84. 84. 
    Lee HO, Davidson JM, Duronio RJ. 2009. Endoreplication: polyploidy with purpose. Genes Dev 23:212461–77
    [Google Scholar]
  85. 85. 
    Lee HS, Kim Y, Pham G, Kim JW, Song JH et al. 2015. Brassinazole resistant 1 (BZR1)-dependent brassinosteroid signalling pathway leads to ectopic activation of quiescent cell division and suppresses columella stem cell differentiation. J. Exp. Bot. 66:154835–49
    [Google Scholar]
  86. 86. 
    Lee LY, Hou X, Fang L, Fan S, Kumar PP, Yu H. 2012. STUNTED mediates the control of cell proliferation by GA in Arabidopsis. Development 139:91568–76
    [Google Scholar]
  87. 87. 
    Lee MG, Nurse P. 1987. Complementation used to clone a human homologue of the fission yeast cell cycle control gene cdc2. Nature 327:611731–35
    [Google Scholar]
  88. 88. 
    Li F, Wang L, Zhang Z, Li T, Feng J et al. 2019. ZmSMR4, a novel cyclin-dependent kinase inhibitor (CKI) gene in maize (Zea mays L.), functions as a key player in plant growth, development and tolerance to abiotic stress. Plant Sci 280:120–31
    [Google Scholar]
  89. 89. 
    Li X, Cai W, Liu Y, Li H, Fu L et al. 2017. Differential TOR activation and cell proliferation in Arabidopsis root and shoot apexes. PNAS 114:102765–70
    [Google Scholar]
  90. 90. 
    López-Juez E, Dillon E, Magyar Z, Khan S, Hazeldine S et al. 2008. Distinct light-initiated gene expression and cell cycle programs in the shoot apex and cotyledons of Arabidopsis. Plant Cell 20:4947–68
    [Google Scholar]
  91. 91. 
    Lozano-Elena F, Planas-Riverola A, Vilarrasa-Blasi J, Schwab R, Caño-Delgado AI. 2018. Paracrine brassinosteroid signaling at the stem cell niche controls cellular regeneration. J. Cell Sci. 131:2jcs204065
    [Google Scholar]
  92. 92. 
    Ma Y, Kanakousaki K, Buttitta L. 2015. How the cell cycle impacts chromatin architecture and influences cell fate. Front. Genet. 6:19
    [Google Scholar]
  93. 93. 
    Magyar Z, Bögre L, Ito M. 2016. DREAMs make plant cells to cycle or to become quiescent. Curr. Opin. Plant Biol. 34:100–6
    [Google Scholar]
  94. 94. 
    Magyar Z, De Veylder L, Atanassova A, Bakó L, Inzé D, Bögre L. 2005. The role of the Arabidopsis E2FB transcription factor in regulating auxin-dependent cell division. Plant Cell 17:92527–41
    [Google Scholar]
  95. 95. 
    Massa AN, Childs KL, Lin H, Bryan GJ, Giuliano G, Buell CR. 2011. The transcriptome of the reference potato genome Solanum tuberosum Group Phureja clone DM1-3 516R44. PLOS ONE 6:10e26801
    [Google Scholar]
  96. 96. 
    Meguro A, Sato Y. 2014. Salicylic acid antagonizes abscisic acid inhibition of shoot growth and cell cycle progression in rice. Sci. Rep. 4:4555
    [Google Scholar]
  97. 97. 
    Menges M, Pavesi G, Morandini P, Bögre L, Murray JA. 2007. Genomic organization and evolutionary conservation of plant D-type cyclins. Plant Physiol 145:41558–76
    [Google Scholar]
  98. 98. 
    Mesa JM, Juvik JA, Paige KN. 2019. Individual and interactive effects of herbivory on plant fitness: endopolyploidy as a driver of genetic variation in tolerance and resistance. Oecologia 190:4847–56
    [Google Scholar]
  99. 99. 
    Minami E, Kuchitsu K, He DY, Kouchi H, Midoh N et al. 1996. Two novel genes rapidly and transiently activated in suspension-cultured rice cells by treatment with N-acetylchitoheptaose, a biotic elicitor for phytoalexin production. Plant Cell Physiol 37:4563–67
    [Google Scholar]
  100. 100. 
    Moreno S, Canales J, Hong L, Robinson D, Roeder AHK, Gutiérrez RA. 2020. Nitrate defines shoot size through compensatory roles for endoreplication and cell division in Arabidopsis thaliana. Curr. Biol. 30:111988–2000
    [Google Scholar]
  101. 101. 
    Nahar N, Rahman A, Nawani NN, Ghosh S, Mandal A. 2017. Phytoremediation of arsenic from the contaminated soil using transgenic tobacco plants expressing ACR2 gene of Arabidopsis thaliana. J. Plant Physiol. 218:121–26
    [Google Scholar]
  102. 102. 
    Nakagami H, Kawamura K, Sugisaka K, Sekine M, Shinmyo A. 2002. Phosphorylation of retinoblastoma-related protein by the cyclin D/cyclin-dependent kinase complex is activated at the G1/S-phase transition in tobacco. Plant Cell 14:81847–57
    [Google Scholar]
  103. 103. 
    Nishida T, Ohnishi N, Kodama H, Komamine A. 1992. Establishment of synchrony by starvation and readdition of auxin in suspension cultures of Catharanthus roseus cells. Plant Cell Tiss. Organ Cult. 28:37–43
    [Google Scholar]
  104. 104. 
    Nowack MK, Harashima H, Dissmeyer N, Zhao X, Bouyer D et al. 2012. Genetic framework of cyclin-dependent kinase function in Arabidopsis. Dev. Cell 22:51030–40
    [Google Scholar]
  105. 105. 
    Ogita N, Okushima Y, Tokizawa M, Yamamoto YY, Tanaka M et al. 2018. Identifying the target genes of SUPPRESSOR OF GAMMA RESPONSE 1, a master transcription factor controlling DNA damage response in Arabidopsis. Plant J 94:3439–53
    [Google Scholar]
  106. 106. 
    Okushima Y, Shimizu K, Ishida T, Sugimoto K, Umeda M. 2014. Differential regulation of B2-type CDK accumulation in Arabidopsis roots. Plant Cell Rep 33:71033–40
    [Google Scholar]
  107. 107. 
    Otero S, Desvoyes B, Peiró R, Gutierrez C. 2016. Histone H3 dynamics reveal domains with distinct proliferation potential in the Arabidopsis root. Plant Cell 28:61361–71
    [Google Scholar]
  108. 108. 
    Pardee AB. 1974. A restriction point for control of normal animal cell proliferation. PNAS 71:41286–90
    [Google Scholar]
  109. 109. 
    Peres A, Churchman ML, Hariharan S, Himanen K, Verkest A et al. 2007. Novel plant-specific cyclin-dependent kinase inhibitors induced by biotic and abiotic stresses. J. Biol. Chem. 282:3525588–96
    [Google Scholar]
  110. 110. 
    Ramirez-Parra E, Gutierrez C. 2007. E2F regulates FASCIATA1, a chromatin assembly gene whose loss switches on the endocycle and activates gene expression by changing the epigenetic status. Plant Physiol 144:1105–20
    [Google Scholar]
  111. 111. 
    Randall RS, Miyashima S, Blomster T, Zhang J, Elo A et al. 2015. AINTEGUMENTA and the D-type cyclin CYCD3;1 regulate root secondary growth and respond to cytokinins. Biol. Open 4:101229–36
    [Google Scholar]
  112. 112. 
    Randall RS, Sornay E, Dewitte W, Murray JA. 2015. AINTEGUMENTA and the D-type cyclin CYCD3;1 independently contribute to petal size control in Arabidopsis: evidence for organ size compensation being an emergent rather than a determined property. J. Exp. Bot. 66:133991–4000
    [Google Scholar]
  113. 113. 
    Richard C, Lescot M, Inzé D, De Veylder L. 2002. Effect of auxin, cytokinin, and sucrose on cell cycle gene expression in Arabidopsis thaliana cell suspension cultures. Plant Cell Tiss. Organ Cult. 69:167–76
    [Google Scholar]
  114. 114. 
    Riou-Khamlichi C, Huntley R, Jacqmard A, Murray JA. 1999. Cytokinin activation of Arabidopsis cell division through a D-type cyclin. Science 283:54071541–44Reveals that cytokinins activate plant cell division by accelerating G1/S progression through induction of CYCD3 expression.
    [Google Scholar]
  115. 115. 
    Riou-Khamlichi C, Menges M, Healy JMS, Murray JA. 2000. Sugar control of the plant cell cycle: differential regulation of Arabidopsis D-type cyclin gene expression. Mol. Cell Biol. 20:4513–21
    [Google Scholar]
  116. 116. 
    Rounds MA, Larsen PB. 2008. Aluminum-dependent root-growth inhibition in Arabidopsis results from AtATR-regulated cell-cycle arrest. Curr. Biol. 18:191495–500
    [Google Scholar]
  117. 117. 
    Sakamoto T, Inui YT, Uraguchi S, Yoshizumi T, Matsunaga S et al. 2011. Condensin II alleviates DNA damage and is essential for tolerance of boron overload stress in Arabidopsis. Plant Cell 23:93533–46
    [Google Scholar]
  118. 118. 
    Sancar A, Lindsey-Boltz LA, Unsal-Kaçmaz K, Linn S 2004. Molecular mechanisms of mammalian DNA repair and the DNA damage checkpoints. Annu. Rev. Biochem. 73:39–85
    [Google Scholar]
  119. 119. 
    Sanz L, Dewitte W, Forzani C, Patell F, Nieuwland J et al. 2011. The Arabidopsis D-type cyclin CYCD2;1 and the inhibitor ICK2/KRP2 modulate auxin-induced lateral root formation. Plant Cell 23:2641–60
    [Google Scholar]
  120. 120. 
    Sas-Nowosielska H, Bernas T. 2016. Spatial relationship between chromosomal domains in diploid and autotetraploid Arabidopsis thaliana nuclei. Nucleus 7:2216–31
    [Google Scholar]
  121. 121. 
    Sauter M. 1997. Differential expression of a CAK (cdc2-activating kinase)-like protein kinase, cyclins and cdc2 genes from rice during the cell cycle and in response to gibberellin. Plant J 11:2181–90
    [Google Scholar]
  122. 122. 
    Schnittger A, Schöbinger U, Bouyer D, Weinl C, Stierhof YD, Hülskamp M 2002. Ectopic D-type cyclin expression induces not only DNA replication but also cell division in Arabidopsis trichomes. PNAS 99:96410–15
    [Google Scholar]
  123. 123. 
    Scholes DR, Paige KN. 2011. Chromosomal plasticity: mitigating the impacts of herbivory. Ecology 92:81691–98
    [Google Scholar]
  124. 124. 
    Schruff MC, Spielman M, Tiwari S, Adams S, Fenby N, Scott RJ. 2006. The AUXIN RESPONSE FACTOR 2 gene of Arabidopsis links auxin signalling, cell division, and the size of seeds and other organs. Development 133:2251–61
    [Google Scholar]
  125. 125. 
    Shimotohno A, Umeda M. 2007. CDK phosphorylation. Cell Cycle Control and Plant Development D Inzé 114–37 Oxford: Wiley-Blackwell
    [Google Scholar]
  126. 126. 
    Smith S, Stillman B. 1989. Purification and characterization of CAF-I, a human cell factor required for chromatin assembly during DNA replication in vitro. Cell 58:115–25
    [Google Scholar]
  127. 127. 
    Song J, Bent AF. 2014. Microbial pathogens trigger host DNA double-strand breaks whose abundance is reduced by plant defense responses. PLOS Pathog 10:4e1004030
    [Google Scholar]
  128. 128. 
    Sozzani R, Cui H, Moreno-Risueno MA, Busch W, Van Norman JM et al. 2010. Spatiotemporal regulation of cell-cycle genes by SHORTROOT links patterning and growth. Nature 466:7302128–32Identifies CYCD6;1 as a target of SCR/SHR in CEI/CEI-daughter cells, providing evidence for cell type–specific cell cycle regulation.
    [Google Scholar]
  129. 129. 
    Spadafora ND, Doonan JH, Herbert RJ, Bitonti MB, Wallace E et al. 2011. Arabidopsis T-DNA insertional lines for CDC25 are hypersensitive to hydroxyurea but not to zeocin or salt stress. Ann. Bot. 107:71183–92
    [Google Scholar]
  130. 130. 
    Swaffer MP, Jones AW, Flynn HR, Snijders AP, Nurse P. 2016. CDK substrate phosphorylation and ordering the cell cycle. Cell 167:71750–61.e16
    [Google Scholar]
  131. 131. 
    Tagami H, Ray-Gallet D, Almouzni G, Nakatani Y 2004. Histone H3.1 and H3.3 complexes mediate nucleosome assembly pathways dependent or independent of DNA synthesis. Cell 116:151–61
    [Google Scholar]
  132. 132. 
    Takahashi N, Inagaki S, Nishimura K, Sakakibara H, Antoniadi I et al. 2020. DNA damage inhibits root growth by enhancing cytokinin biosynthesis in Arabidopsis thaliana. bioRxiv 2020.06.19.160838. https://doi.org/10.1101/2020.06.19.160838
    [Crossref]
  133. 133. 
    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. 23:181812–17
    [Google Scholar]
  134. 134. 
    Takahashi N, Ogita N, Takahashi T, Taniguchi S, Tanaka M et al. 2019. A regulatory module controlling stress-induced cell cycle arrest in Arabidopsis. eLife 8:e43944Identifies ANAC044/ANAC085-Rep-MYB as a core module controlling G2 arrest in response to multiple stresses.
    [Google Scholar]
  135. 135. 
    Tan S, Sanchez M, Laffont C, Boivin S, Le Signor C et al. 2020. A cytokinin signalling type-B response regulator transcription factor acting in early nodulation. Plant Physiol 183:31319–30
    [Google Scholar]
  136. 136. 
    Taniguchi M, Sasaki N, Tsuge T, Aoyama T, Oka A. 2007. ARR1 directly activates cytokinin response genes that encode proteins with diverse regulatory functions. Plant Cell Physiol 48:2263–77
    [Google Scholar]
  137. 137. 
    Umeda M, Aki SS, Takahashi N. 2019. Gap 2 phase: making the fundamental decision to divide or not. Curr. Opin. Plant Biol. 51:1–6
    [Google Scholar]
  138. 138. 
    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]
  139. 139. 
    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 14:4903–16
    [Google Scholar]
  140. 140. 
    Verkest A, Manes CL, Vercruysse S, Maes S, Van Der Schueren E et al. 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 17:61723–36
    [Google Scholar]
  141. 141. 
    Vilarrasa-Blasi J, González-García MP, Frigola D, Fàbregas N, Alexiou KG et al. 2014. Regulation of plant stem cell quiescence by a brassinosteroid signaling module. Dev. Cell 30:136–47
    [Google Scholar]
  142. 142. 
    Vinardell JM, Fedorova E, Cebolla A, Kevei Z, Horvath G et al. 2003. Endoreduplication mediated by the anaphase-promoting complex activator CCS52A is required for symbiotic cell differentiation in Medicago truncatula nodules. Plant Cell 15:92093–105
    [Google Scholar]
  143. 143. 
    Waterworth WM, Footitt S, Bray CM, Finch-Savage WE, West CE 2016. DNA damage checkpoint kinase ATM regulates germination and maintains genome stability in seeds. PNAS 113:349647–52
    [Google Scholar]
  144. 144. 
    Weimer AK, Matos JL, Sharma N, Patell F, Murray JAH et al. 2018. Lineage- and stage-specific expressed CYCD7;1 coordinates the single symmetric division that creates stomatal guard cells. Development 145:6dev160671
    [Google Scholar]
  145. 145. 
    Xie Z, Lee E, Lucas JR, Morohashi K, Li D et al. 2010. Regulation of cell proliferation in the stomatal lineage by the Arabidopsis MYB FOUR LIPS via direct targeting of core cell cycle genes. Plant Cell 22:72306–21
    [Google Scholar]
  146. 146. 
    Xiong Y, McCormack M, Li L, Hall Q, Xiang C, Sheen J. 2013. Glucose–TOR signalling reprograms the transcriptome and activates meristems. Nature 496:7444181–86Provides evidence to connect the photosynthesis-derived glucose signal and the cell cycle through the TOR signaling pathway.
    [Google Scholar]
  147. 147. 
    Xu P, Zhao P-X, Cai X-T, Mao J-L, Miao Z-Q, Xiang C-B. 2020. Integration of jasmonic acid and ethylene into auxin signaling in root development. Front. Plant Sci. 11:271
    [Google Scholar]
  148. 148. 
    Yi D, Alvim Kamei CL, Cools T, Vanderauwera S, Takahashi N 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 26:1296–309
    [Google Scholar]
  149. 149. 
    Yoshiyama KO. 2015. SOG1: a master regulator of the DNA damage response in plants. Genes Genet. Syst. 90:4209–16
    [Google Scholar]
  150. 150. 
    Yoshiyama KO, Conklin PA, Huefner ND, Britt AB 2009. Suppressor of gamma response 1 (SOG1) encodes a putative transcription factor governing multiple responses to DNA damage. italicPNAS 1063112843–48
  151. 151. 
    Yoshiyama KO, Kobayashi J, Ogita N, Ueda M, Kimura S et al. 2013. ATM-mediated phosphorylation of SOG1 is essential for the DNA damage response in Arabidopsis. EMBO Rep 14:9817–22
    [Google Scholar]
  152. 152. 
    Zhao L, Wang P, Hou H, Zhang H, Wang Y et al. 2014. Transcriptional regulation of cell cycle genes in response to abiotic stresses correlates with dynamic changes in histone modifications in maize. PLOS ONE 9:8e106070
    [Google Scholar]
  153. 152a. 
    Zhiponova MK, Pettkó-Szandtner A, Stelkovics E, Neer Z, Bottka Set al 2006. Mitosis-specific promoter of the alfalfa cyclin-dependent kinase gene (Medsa;CDKB2;1) is activated by wounding and ethylene in a non-cell division-dependent manner. Plant Physiol 140:693703
    [Google Scholar]
  154. 153. 
    Zhou W, Lozano-Torres JL, Blilou I, Zhang X, Zhai Q et al. 2019. A jasmonate signaling network activates root stem cells and promotes regeneration. Cell 177:4942–56
    [Google Scholar]
/content/journals/10.1146/annurev-arplant-080720-103739
Loading
/content/journals/10.1146/annurev-arplant-080720-103739
Loading

Data & Media loading...

Supplemental Material

Supplementary Data

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error