Mechanisms of endosperm initiation

Abstract

Overview of developmental events and signalling during central cell maturation and early endosperm development with a focus on mechanisms of sexual and autonomous endosperm initiation. Endosperm is important for seed viability and global food supply. The mechanisms regulating the developmental transition between Female Gametophyte (FG) maturation and early endosperm development in angiosperms are difficult to study as they occur buried deep within the ovule. Knowledge of the molecular events underlying this developmental window of events has significantly increased with the combined use of mutants, cell specific markers, and plant hormone sensing reporters. Here, we review recent discoveries concerning the developmental events and signalling of FG maturation, fertilization, and endosperm development. We focus on the regulation of the initiation of endosperm development with and without fertilization in Arabidopsis and the apomict Hieracium, comparing this to what is known in monocots where distinct differences in developmental patterning may underlie alternative mechanisms of suppression and initiation. The Polycomb Repressive Complex 2 (PRC2), plant hormones, and transcription factors are iteratively involved in early fertilization-induced endosperm formation in Arabidopsis. Auxin increases and PRC2 complex inactivation can also induce fertilization-independent endosperm proliferation in Arabidopsis. Function of the PRC2 complex member FERTILIZATION-INDEPENDENT ENDOSPERM and two loci AutE and LOP are required for autonomous endosperm development in apomictic Hieracium. A comparative understanding of cues required for early endosperm development will facilitate genetic engineering approaches for the development of resilient seed crops, especially if an option for fertilization-independent endosperm formation was possible to combat stress-induced crop failure.

Keywords: Development; Endosperm; Female gametophyte; Fertilization.

Fig. 1

Arabidopsis female gametophyte and early endosperm development. Processes and events of Arabidopsis FG maturation, endosperm initiation, and early development. A Following FG cellularization, the two PN are sequestered to the CC and migrate towards the egg cell. Upon meeting the PN fuse to generate the SN positioned adjacent to the egg cell nuclei. PN fusion is the final event of FG development after which the SN is mitotically arrested until fertilisation. B Fertilization. Pollen tube penetration of the receptive synergid triggers cell death. Rupture releases the sperm cells which individually fuse with egg and CC. In the CC, nuclear proliferation begins rapidly after fertilization. Antipodal cell degeneration begins at this stage along with cytoplasmic fusion of the persistent synergid with CC. C Endosperm development. Rapid acytokinetic mitosis in the CC occurs accompanied by nuclear migration from the mycropylar to chalazal pole. CC and vacuole enlarge rapidly resulting in nuclei distributed around the periphery of the CC. Cellularization occurs with ongoing mitosis progressing from the CC periphery towards the centre until complete. Key process occurring during each stage are listed in diagrams below. PN polar nuclei, SN secondary nucleus, S synergid cell, rS receptive synergid, pS persistent synergid, E egg cell, A antipodal cells, CC central cell, FG female gametophyte

Fig. 2

Diagram of signalling events of Arabidopsis fertilisation and endosperm initiation. Procession of the events and signalling involved in fertilization and endosperm developmental initiation in Arabidopsis. Pollen tube rupture in the degenerating synergid releases the sperm cells. Associated calcium signalling triggers the release of EC1 peptides involved in sperm cell activation and potentially auxin influx to the CC. Individual sperm cells fuse with E and CC (Plasmogamy) followed by fusion of their respective nuclei (Karyogamy). In the CC maternal auxin biosynthesis, genes are repressed by the FIS-PRC2. Nuclear fusion in the CC initiates paternal gene expression, which results in auxin biosynthesis and increase in the CC that may also include auxin influx. In conjunction with AGL62 activity, increased auxin concentration triggers the release of mitotic arrest mechanisms and nuclear proliferation in the CC. Nuclear fusion in the egg cell triggers calcium signalling associated with rapid polyspermy blockade along with ethylene biosynthesis responsible for triggering plasmogamy of the persistent synergid with the CC and polytubey blockade. Solid black arrows indicate reported signalling events. Blue-dotted arrows represent proposed signalling events