Cell cycle control and seed development

Abstract

Seed development is a complex process that requires coordinated integration of many genetic, metabolic, and physiological pathways and environmental cues. Different cell cycle types, such as asymmetric cell division, acytokinetic mitosis, mitotic cell division, and endoreduplication, frequently occur in sequential yet overlapping manner during the development of the embryo and the endosperm, seed structures that are both products of double fertilization. Asymmetric cell divisions in the embryo generate polarized daughter cells with different cell fates. While nuclear and cell division cycles play a key role in determining final seed cell numbers, endoreduplication is often associated with processes such as cell enlargement and accumulation of storage metabolites that underlie cell differentiation and growth of the different seed compartments. This review focuses on recent advances in our understanding of different cell cycle mechanisms operating during seed development and their impact on the growth, development, and function of seed tissues. Particularly, the roles of core cell cycle regulators, such as cyclin-dependent-kinases and their inhibitors, the Retinoblastoma-Related/E2F pathway and the proteasome-ubiquitin system, are discussed in the contexts of different cell cycle types that characterize seed development. The contributions of nuclear and cellular proliferative cycles and endoreduplication to cereal endosperm development are also discussed.

Keywords: cell division; cotyledon; cyclin-dependent kinase; embryo; endoreduplication; endosperm; retinoblastoma-related; seed coat.

FIGURE 1

Cell cycle types occurring during seed development. Triploid endosperm mother cells (with two maternal and one paternal chromosomal complements) are shown as an example. A hypothetical haploid number n = 1 is assumed for simplicity. (A) Acytokinetic mitosis of endosperm nuclei within the embryo sac central cell, resulting in a syncytium; (C) Cell proliferation through mitotic cell division following syncytium cellularization; (E) Endoreduplication of inner endosperm starchy cells. Cell number, size, DNA content, and chromosome number correspond to one complete cell cycle round comprising S-phase and accompanying M-phase and karyokinesis (A,C) and cytokinesis (C), and two complete endoreduplication cycle rounds (each comprising S-phase not followed by M-phase, karyokinesis and cytokinesis) (E). Interrupted cell boundaries in (A) indicate the large size of the embryo sac central cell. C and n, DNA content and chromosome number of a haploid cell, respectively. (B,D,F) show typical nuclear flow-cytometric profiles obtained for tissues undergoing asynchronous, iterative acytokinetic mitosis, mitotic cell division, and endoreduplication cycles, respectively.

FIGURE 2

The prototypical mitotic cell division cycle and some key molecular mechanisms that regulate its major transitions in plants. Cell cycle progression through distinct phases is driven by periodic fluctuations of cyclin-dependent kinase (CDK) activity (solid red line). Green and red circles labeled with a P letter show stimulatory and inhibitory phosphorylation, respectively. For cells to make a transition from G1 into S-phase and execute DNA replication, CDK activity must surpass an S-phase threshold (dashed blue line). A further CDK activity increase above an M-phase threshold (dashed green line) during G2 drives entry into mitosis. Both M-phase exit and origin of replication licensing require CDK activity to be reduced at the end of mitosis and maintained at low levels for most of G1. At the G1/S transition, CDKA/CYCD complexes phosphorylate and thus inactivate retinoblastoma-related (RBR), thus permitting heterodimeric E2F/DP transcription factors to stimulate an S-phase gene expression program, which results in the expression of MCM2-7 and proliferating cell nuclear antigen (PCNA) genes, among many others. CDKA/CYCD activity is positively and negatively regulated by, respectively, CDK-activating kinase (CAK)-dependent phosphorylation and binding by CKIs. Later in G2, CDK activity requires association with mitotic cyclins and is also stimulated by CAK and inhibited by CKIs. In addition, this CDK activity is inhibited by phosphorylation at specific tyrosine residues by WEE1. Certain CDKs of the B-type, whose expression is E2F/DP-dependent, promote M-phase progression by mechanisms that include interaction with A-type cyclins and stimulation of downstream CDK activity by phosphorylating and targeting certain CKIs for proteolysis by the ubiquitin-proteasome system (UPS) via different E3 ubiquitin ligases. Conversely, mitotic cyclin proteolysis by the UPS, via the APC/C, causes CDK activity to decline sharply, which is required for M-phase exit.

FIGURE 3

Effects of core cell cycle regulators on the cereal endosperm cell cycles. Core cell cycle regulators that positively or negatively regulate proliferative (acytokinetic mitosis and mitotic cell division) and endoreduplication cycles are shown. Net stimulatory or inhibitory effects are assigned as a function of cell proliferation- and ploidy-related phenotypes observed in mutant or transgenic analyses carried out either in planta or plant cell cultures (red-colored fonts) or inferred from a combination of expression analyses and biochemical assays (black-colored fonts), as discussed in the text. Os, Oryza sativa; Zm, Zea mays.