A positive signal from the fertilization of the egg cell sets off endosperm proliferation in angiosperm embryogenesis

Abstract

Double fertilization of the egg cell and the central cell by one sperm cell each produces the diploid embryo and the typically triploid endosperm and is one of the defining characteristics of flowering plants (angiosperms). Endosperm and embryo develop in parallel to form the mature seed, but little is known about the coordination between these two organisms. We characterized a mutation of the Arabidopsis thaliana Cdc2 homolog CDC2A (also called CDKA;1), which has a paternal effect. In cdc2a mutant pollen, only one sperm cell, instead of two, is produced. Mutant pollen is viable but can fertilize only one cell in the embryo sac, allowing for a genetic dissection of the double fertilization process. We observed exclusive fertilization of the egg cell by cdc2a sperm cells. Moreover, we found that unfertilized endosperm developed, suggesting that a previously unrecognized positive signal from the fertilization of the egg cell initiates proliferation of the central cell.Plants have a complex life cycle involving the alternation of a diploid sporophytic and a haploid gametophytic phase. In flowering plants, the female spore (megaspore), generated from the sporophyte, typically develops through a series of syncytial nuclear divisions followed by 'cellularization' into a seven-celled female gametophyte (embryo sac) comprising three antipodals, two synergids, a binucleated central cell and the egg cell 1 . The male spore (microspore) undergoes a defined cell division program resulting in a male gametophyte (pollen grain) comprising a vegetative cell that encloses two sperm cells 2 .Cell divisions in plants, as in other higher eukaryotes, are controlled by a class of serine-threonine kinases called cyclin-dependent kinases (CDKs). Some of the central CDKs in plants are A-type CDK proteins. A. thaliana contains only one A-type CDK, called CDC2A (or CDKA;1), which can rescue the fission yeast cdc2 mutant [3][4][5] . Previous studies with dominant negative variants showed that CDC2A activity is required for entering both mitosis and the DNA synthesis-phase in A. thaliana, maize and tobacco [6][7][8] .

Growth coordination and the shoot epidermis

“…However, such a scenario won't be able to rescue the high inhibitory activity of KRP1/ICK1. In this regard, it would be interesting to test the reciprocal situation in which ICK targets (CDKs) are depleted from the L1 (for example by deletion sectors of CDKA;1 [28,29]). In any case (it could be a signal, or it could be movement of wild type HBT or its targets), the rescue signal of cell division in the HBT experiment comes from the L2/L3 layers.…”

Endosperm: an integrator of seed growth and development

“…In cdka;1 mutant pollen, the generative cell fails to enter PMII and remains in the G 2 phase with a DNA content of about 2C [9 ,10]. Importantly, this mutant pollen is able to complete fertilization [9 ]. To prevent aneuploidy and allow proper development of the zygote, the two nuclei of the gametes need to fuse in the same cell cycle phase.…”

“…Proper differentiation of both female gametes might involve the function of RBR1. A recent report [9 ] on a functional knock-out of the Arabidopsis CDKA1;1 has provided evidence for mechanisms that might be involved in cell-cycle control prior to fertilization.…”

“…However, this observation indicates some kind of communication from the endosperm to the embryo. Communication from the embryo to the endosperm has been revealed by analysis of the mutant for the Arabidopsis homolog of the cyclin dependent kinase cdc2a, CDKA;1 [9 ]. In heterozygous cdka;1 null mutants, 50% of the pollen contain a single sperm cell [9 ,10] that exclusively fertilizes the egg cell.…”

Networks controlling seed size in Arabidopsis

“…The failure of 111 karyogamy in the central cell has been shown to impair 112 endosperm development causing seed abortion (Aw et al 113 2010). Interestingly, viable seeds can also be produced in 114 the presence of homoparental diploid, as opposed to trip-115 loid, endosperm (Nowack et al 2006(Nowack et al , 2007. In cdka;1 116 mutants, pollen fertilizes only the egg cell, not the central 117 cell due to karyogamy failure (Aw et al 2010).…”