Cell cycle arrest in plants

In the cell cycle, the G1 phase can be like a prison, where plant cells are arrested, unable to divide. These cells have been arrested for different reasons, serving sentences of different lengths. So how and why did they get there?

Recently, Velappan et al. reviewed cell cycle arrest in plants, focussing on three types; meristem quiescence, dormancy and terminal differentiation. What is it that causes quiesence?

G1 – It’s just a phase

Mitosis is a fundamental process that governs the duplication of chromosomes, followed by the division of a single cell to form two genetically identical daughter cells. The mitotic cell cycle is essential in all multicellular organisms for development, growth and cell replacement.

Diagram showing the common stages of the cell cycle.
Diagram showing the common stages of the cell cycle. The mitotic phase usually takes up about 10% of the time. M = mitosis, C = cytokinesis, G1 = gap phase 1, S = synthesis phase, G2 = gap phase 2. Image: George Weller / Wikipedia

The plant cell cycle, like all eukaryotic cells, contains a sequence of regulated phases, including DNA synthesis (S), mitosis (M) and two gap phases, namely G1 and G2.

The S phase and gap phases are stages in which the cell is not dividing, collectively known as interphase. This period is longest phase of the cell cycle and allows the cell to grow and prepare for division in mitosis.

The main function of the G1 stage is to prepare nuclei for DNA synthesis in the S phase. In G1, the cell accomplishes the majority of its growth, along with the synthesis of mRNA and proteins required in subsequent steps.

The G1 phase also acts as a crucial checkpoint, allowing cells to decide whether they can truly commit to mitotic division. Cells can become arrested in G1, essentially exiting the cell cycle. In plants, these cells are described as quiescent. Control between cell quiescence and proliferation allows them to respond to factors, such as nutritional availability and abiotic/biotic stress.

Major distinguishing regulators defining the decision of a dividing cell to quiesce, differentiate or enter dormancy.
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. Source: Velappan et al. 2017

Velappan et al. review three types of cell cycle arrest in plants, which have clear differences in physiology. However, they are all commonly referred to as cells under ‘G1 arrest’. Despite being largely characterised by G1 arrest, meristematic quiescence, dormancy and terminal differentiation are all regulated distinctly.

Meristematic Quiescence – Replenishing the Undifferentiated

Meristematic quiescence is the repression of division in undifferentiated cells of a plant’s meristem.

A plant’s meristem is it’s own personal resource of pluripotent stem cells. These cells are undifferentiated and can divide to become several different cell types. The apical meristem tissue consists of actively dividing cells, found at the tips of roots and stems. The root and shoot apical meristem (RAM, SAM), have an organising centre (OC) and quiescent centre (QC), respectively. These centres are reservoirs of quiescent cells, essential for the maintenance and replenishment of pluripotent stem cells.

Plants regulate meristematic quiescence in a number of ways. One method of regulation relies on redox and oxygen-dependent reactions. Reactive Oxygen Species (ROS) and redox signalling can determine the extent of quiescence and proliferation in the RAM and SAM. For example, the oxidation of antioxidants, ascorbate and glutathione, is highly linked to G1 arrest in the QC cells of RAM.

There is also evidence that meristem quiescence is linked to abscisic acid, a stress-related signalling molecule and mitotic inhibitor.

Dormancy – Sleeping through the Bad Weather

In plant physiology, dormancy evolved as a survival strategy. Dormancy can be switched on in different plant organs, such as seeds and buds, and is regulated by both genetic and environmental factors.

In response to unfavourable conditions, such as freezing temperatures, cells can become arrested in the G1 phase to inhibit cell growth and development. By halting cell division, the plant can conserve energy when conditions are unsuitable for growth.

Regulation dormancy in plant cells relates to the level of chromatin accessibility, which is regulated by histone modifications of dormancy genes.

The Polycomb group (PcG) and Trithorax group (TrxG) are two complexes that determine chromatin state during quiescence and proliferation of cells. The PcG complex inhibits gene activity by inducing a heterochromatin state associated with nuclear quiescence. The TrxG complex induces a more euchromatic state in the cell, which is ideal for active transcription. These two complexes regulate dormancy in plant cells through their modification of dormancy genes.

Terminal Differentiation – Saying Goodbye to the Cell Cycle

Terminal differentiation, also known as cell cycle exit, is a process in which pluripotent stem cells become differentiated into particular cell types. These different cell types have specific functions within the organism.

Proliferation arrest is linked to cells with distinct cell fates, formed through asymmetrical division in undifferentiated cells. G1 arrest is important in the process of terminal differentiation, since G1 is the phase in which commitment to differentiation is induced.

Regulation of terminal differentiation shares similarities with the control of meristematic quiescence. For example, research has determined that ROS levels also play a role in cell fate and commitment to differentiation. In most root cells, proliferation and elongation is controlled by O2·- and H2O2, respectively. This appears to be essential to a cell’s commitment to differentiate. Despite similarities, terminal differentiation has different activators to meristematic quiescence and a higher dependence on cytokinin signalling.

 

The three types of cellular quiescence are achieved through different molecular pathways, but all lead to G1 arrest. There are other cells locked in G1 too, such as those in senescence and stress-induced quiescence.

As research continues and evidence arises, we can hope to get a better picture of how and why these cells are locked up in a G1 prison. This will undoubtedly deepen our understanding of plant developmental and stress biology, whilst also contributing to other aspects of agriculture and ecology, such as darkness and nutrient limitation.

 

Reference List

Velappan, Y., Signorelli, S., & Considine, M. J. (2017). Cell cycle arrest in plants: what distinguishes quiescence, dormancy and differentiated G1? Annals of Botany, 120(4), 495–509. https://doi.org/10.1093/aob/mcx082