Mutations in FIE, a WD Polycomb Group Gene, Allow Endosperm Development without Fertilization

Abstract

A fundamental problem in biology is to understand how fertilization initiates reproductive development. Higher plant reproduction is unique because two fertilization events are required for sexual reproduction. First, a sperm must fuse with the egg to form an embryo. A second sperm must then fuse with the adjacent central cell nucleus that replicates to form an endosperm, which is the support tissue required for embryo and/or seedling development. Here, we report cloning of the Arabidopsis FERTILIZATION-INDEPENDENT ENDOSPERM ( FIE ) gene. The FIE protein is a homolog of the WD motif-containing Polycomb proteins from Drosophila and mammals. These proteins function as repressors of homeotic genes. A female gametophyte with a loss-of-function allele of fie undergoes replication of the central cell nucleus and initiates endosperm development without fertilization. These results suggest that the FIE Polycomb protein functions to suppress a critical aspect of early plant reproduction, namely, endosperm development, until fertilization occurs. INTRODUCTIONThe higher plant life cycle alternates between multicellular haploid (i.e., gametophyte) and diploid (i.e., sporophyte) generations. In Arabidopsis, the ovule generates the female gametophyte, which is composed of egg, central, synergid, and antipodal cells ( Figure 1A). Surrounding and protecting the female gametophyte are maternal cell layers, which are called the integuments ( Figure 1A). Double fertilization within the female gametophyte activates four reproductive developmental programs. (1) The fertilized egg initiates embryogenesis ( Figure 1D). (2) The fertilized central cell generates the primary triploid endosperm nucleus that replicates to form the endosperm ( Figure 1D), which is the tissue that supports the development of the embryo. (3) The maternal integument cell layers of the ovule become the seed coat ( Figures 1D and 1H). (4) The ovary differentiates and elongates to form the fruit, or silique ( Figure 1F).The two products of fertilization, embryo and endosperm, display distinct patterns of development. In Arabidopsis, the embryo proceeds through a series of stages that have been defined morphologically as preglobular, globular ( Figure 1D), heart, cotyledon, and maturation ( Figure 1H). During these stages, an axis of polarity is fixed, shoot and root meristems are formed, and storage organs are generated (Goldberg et al., 1994). In contrast, the fertilized central cell (i.e., the primary endosperm nucleus) divides mitotically to produce a syncytium of nuclei that fills an expanding central cell (Figure 1D). After cytokinesis occurs, endosperm cells produce storage proteins, starch, and lipids (Lopes and Larkins, 1993).Ultimately, the endosperm is absorbed by the developing embryo ( Figure 1H). It is thought that endosperm evolved from a supernumerary fertilization event that originally produced multiple embryos and may represent a highly modified embryo that enhances the fitness of its sister embryo (Friedman, 1992(Friedman, , 1995.To understand t...

Endosperm: an integrator of seed growth and development

“…The Pc-G complex FERTILIZATION INDEPENDENT SEED (FIS) contains the SET domain protein MEDEA (MEA) [11], the VEFS domain protein FIS2 [12], and the WD40 domain protein FERTILIZA-TION INDEPENDENT ENDOSPERM (FIE) [13]. Loss-of-function mutations of FIS genes cause autonomous onset of cell division in the central cell in the absence of fertilization [14,15].…”

Genetic mechanisms of apomixis

“…FIS3/FIE encodes a Polycomb group protein that participates in a complex involved (like DNA methylation) in gene silencing (Luo et al 1999;Ohad et al 1999). If an ovule carrying a fie-1 mutation is pollinated, there is dramatic overproliferation of endosperm reminiscent of the lethal paternal excess phenotype seen in 2x´6x crosses (figure 5a), and the embryo arrests by torpedo stage.…”

Plant SET domain-containing proteins: Structure, function and regulation

“…In Arabidopsis, the involvement of MEA, CLF and SWN in developmental processes may be linked to their interactions with other non-SET proteins, as mutations in the interacting partners display phenotypes indicative of affecting similar developmental pathways. During seed development, MEA is part of a PcG complex that includes several other regulators of early seed development such as FERTILIZATION-INDEPENDENT ENDOSPERM (FIE) and FERTILIZATION-INDEPENDENT SEED2 (FIS2) [110][111][112]. FIE is a WD40 domain-containing protein that shows similarity to the Drosophila EXTRA SEX COMB (ESC).…”