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Review
. 2017 Oct 17;120(4):495-509.
doi: 10.1093/aob/mcx082.

Cell cycle arrest in plants: what distinguishes quiescence, dormancy and differentiated G1?

Yazhini Velappan  1   2 , Santiago Signorelli  1   2   3 , Michael J Considine  1   2   4   5
Affiliations
Review

Cell cycle arrest in plants: what distinguishes quiescence, dormancy and differentiated G1?

Yazhini Velappan et al. Ann Bot. .

Abstract

Background: Quiescence is a fundamental feature of plant life, which enables plasticity, renewal and fidelity of the somatic cell line. Cellular quiescence is defined by arrest in a particular phase of the cell cycle, typically G1 or G2; however, the regulation of quiescence and proliferation can also be considered across wider scales in space and time. As such, quiescence is a defining feature of plant development and phenology, from meristematic stem cell progenitors to terminally differentiated cells, as well as dormant or suppressed seeds and buds. While the physiology of each of these states differs considerably, each is referred to as 'cell cycle arrest' or 'G1 arrest'.

Scope: Here the physiology and molecular regulation of (1) meristematic quiescence, (2) dormancy and (3) terminal differentiation (cell cycle exit) are considered in order to determine whether and how the molecular decisions guiding these nuclear states are distinct. A brief overview of the canonical cell cycle regulators is provided, and the genetic and genomic, as well as physiological, evidence is considered regarding two primary questions: (1) Are the canonical cell cycle regulators superior or subordinate in the regulation of quiescence? (2) Are these three modes of quiescence governed by distinct molecular controls?

Conclusion: Meristematic quiescence, dormancy and terminal differentiation are each predominantly characterized by G1 arrest but regulated distinctly, at a level largely superior to the canonical cell cycle. Meristematic quiescence is intrinsically linked to non-cell-autonomous regulation of meristem cell identity, and particularly through the influence of ubiquitin-dependent proteolysis, in partnership with reactive oxygen species, abscisic acid and auxin. The regulation of terminal differentiation shares analogous features with meristematic quiescence, albeit with specific activators and a greater role for cytokinin signalling. Dormancy meanwhile appears to be regulated at the level of chromatin accessibility, by Polycomb group-type histone modifications of particular dormancy genes.

Keywords: Dormancy; branching; cell cycle; chromatin; differentiation; hormone; meristem; mitosis; proliferation; quiescence; reactive oxygen species; ubiquitin-dependent proteolysis.

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Figures

F<sc>ig</sc>. 1.
Fig. 1.
Canonical cell cycle regulation in plants. The cell cycle comprises four principal phases: DNA synthesis (S), mitosis (M) and two intervening gap phases (G1, G2), plus a theoretical quiescent phase (G0). Growth-promoting factors promote formation of the CYCD/CDKA complex, which, when activated by CDKF and CDKD in association with CYCH (CAK pathway), causes phosphorylation of RBR, thus activating the E2F/DP complex, which encourages the transcription necessary to cause G1/S transition. CYCAs are synthesized during the S phase, which, in complex with CDKAs, promotes transition to G2. CYCA/B in complex with CDKA and CDKB under the regulation of the CAK pathway acts at the G2/M check-point to regulate G2/M transition. WEE1 kinase suppresses the G2/M transition in response to DNA damage. In the absence of growth-promoting conditions, cells restrict growth in G0 but resume growth when favourable conditions become available. Differentiated and/or senescent G0 cells are rarely capable of re-entering the cell cycle. In animals, it has been proposed that cells can only enter G0 prior to the restriction point (R), but after passing R are committed to the cell cycle; as yet the evidence for this restriction point is lacking in plants. Mitotic inhibitors are capable of inactivating the CYC/CDK complexes by stimulating CKIs like KRP, causing cell cycle arrest at the check-points. KRP can be inactivated by CDKB kinase activity, causing an increase in CDK activity during mitosis. + and – indicate promotion and inhibition of the pathways, respectively. For simplification, P indicates either ATP (when it is used as substrate) or phosphate (when it is linked to a molecule). CDKs, cyclin-dependent kinases; CYCs, cyclins; CKI, cyclin-dependent kinase inhibitor; KRP, kip-related proteins; RBR, retinoblastoma-related protein.
F<sc>ig</sc>. 2.
Fig. 2.
Regulation of hormone control of the G1/S transition during dormancy by chromatin regulators. (A) In the dormant state most of the cells have 2C DNA, so it is considered that there is strong regulation of the G1/S transition. RBR mediates the repression of genes involved in the S phase. Abscisic acid (ABA) induces the activity of CDKA inhibitors, KRP1 (ICK1) and KRP2 (ICK2), inhibiting G1/S transition. Although it is suggested that ethylene (ET) and ABA are antagonistic, the signalling cascade induced by ET has also been suggested to repress CDKA activity. The histone deacetylation mediated by SNL1 and SNL2 is suggested to promote this ABA–ethylene antagonism. This modification would be relevant in the dormant state. (B) Histone demethylation, mediated by LDL1 and LDL2, would have implications for dormancy release by reducing ABA signalling (by repressing the expression of ABA2, ABI3 and ABI5). Cytokinins (CK) induce CYCD both by themselves and by inducing nitric oxide (•NO) accumulation. GA represses the CDK inhibitors and promotes CYC and FT, which is suggested to induce CDK. Moreover, ET induces gibberellic acid (GA) signalling. In such a situation the complex CYCD/CDKA is able to phosphorylate RBR, allowing the expression of genes involved in S phase. Hence the non-dormant state is characterized by the presence of a greater G1:G2 ratio. CAK, CDK-activating kinases; CDK, cyclin dependent kinases; CYC, cyclins; LDL, lysine-specific demethylase like; RBR, retinoblastoma related protein; SNL, SIN3-like.
F<sc>ig</sc>. 3.
Fig. 3.
Major distinguishing regulators defining the decision of a dividing cell to quiesce, differentiate or enter dormancy. Regulated proteolysis of transcription factors and other unknown targets by APC/C E3 ligase, activated by CCS52A2, operates in partnership with an oxidized cellular state (ROS), abscisic acid (ABA) signalling and cyclin-dependent kinase inhibitors (KRP) to define meristematic quiescence. In a similar way, regulated proteolysis by the APC/C, activated by CCS52A1, regulates the commitment to differentiation in partnership with the regulated balance of H2O2 and O2•− and cytokinin signalling. By contrast, dormancy is regulated at the level of chromatin accessibility, by the action of PcG-type histone modifications. Further details are given in the text.
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