Control of seed size in plants.

R eproductive success in seed plants depends on a healthy seed set. The viability of the embryo is enhanced if a seed contains substantial reserves of starch and protein to nourish the seedling when it germinates months or years later in uncertain conditions. Increased reserves will generally result in an increased seed size, but large seeds are less efficiently dispersed, unless there is human or other intervention. Since the beginning of agriculture, food grains have been subjected to selection and breeding for size as well as for other qualities, and most of the grains consumed today have seeds far larger than their wild relatives. Although grain size has been much analyzed and used by plant breeders over the past century, it is only in the past decade that we have at last begun to identify the molecular regulators of seed size in plants, mainly from studies in the model plant Arabidopsis (reviewed in ref. 1). The article by Luo et al. (2) in a recent issue of PNAS marks another step toward understanding the nature of these controls. The life cycle of plants involves an alternation of generations between the haploid gametophyte and the diploid sporophyte. In angiosperms (flowering plants), seed development begins with double fertilization. Pollen grains (male gametophytes) carry two haploid sperm cells, which fertilize the egg cell and the central cell of the haploid embryo sac (female gametophyte) contained within the maternal tissues of the ovule. This event results in the formation of the diploid embryo and the triploid endosperm, respectively, the latter arising from the central cell that contains two identical haploid sets of chromosomes. Seed development is marked by the rapid growth of the endosperm and the embryo, until seed maturation, which is accompanied by desiccation. Simultaneously, the maternal ovule also undergoes regulated growth to accommodate the growing embryo and endosperm, and the integuments of the ovule ultimately constitute the coat of the mature seed (Fig. 1). The endosperm grows much more rapidly than the embryo, growing initially through nuclear divisions as a syncitium for several mitotic cycles and subsequently cellularizing followed by decreased rate of growth. The growth of the seed is coupled with the growth of the endosperm, with the major increase in seed volume occurring in concordance with the rapid growth of the endosperm. In monocots and some dicots, the endosperm constitutes the major contribution to the volume of the mature seed. In Arabidopsis and many other dicots, the endosperm is eventually consumed, being replaced by the growing embryo, which then constitutes most of the mature seed. However, in all cases the growth of the seed is primarily associated with the initial growth of the endosperm, and not with the later growth of the embryo. Thus, the size of the seed is the result of three different growth programs: those of the diploid embryo, the triploid endosperm, and the diploid maternal ovule. The control and coordination of these growth programs are under genetic regulation as described below. Differences in the contributions of maternal and paternal genomes to seed size are evident from experiments that alter gene dosage through crosses between diploid and tetraploid plants (3, 4). Such crosses show that when the paternal genome is in excess, seed growth is promoted, and conversely, excess of the maternal genome results in smaller seeds. Models to account for these ‘‘parent-of-origin’’ effects have been proposed, based either on theories of ‘‘genome conflict’’ (3) or on differential dosage (4). These parent-of-origin effects on seed development appear to act primarily through regulation of endosperm growth (1). If seed growth involves coordinated growth control of ovule and seed, we may predict that mutants causing reduced seed size would result in reduction of integument growth. It has long been known that embryo lethal mutants can result in smaller seeds with reduced seed coats, but the arrested growth of the integuments could be a general response to embryo arrest and death, rather than a specific control of integument growth rate. Recently, a class of reduced seed size mutants called haiku mutants has been characterized (5, 6), in which embryo and endosperm growth are reduced but not arrested, and the seeds remain viable. Plants grown from homozygous haiku mutant seeds are normal, indicating that these genes might specifically function in seed growth. Detailed analysis of the haiku mutants showed that they appear to be primarily restricting endosperm growth, and that integument cell elongation is reduced as a result. Interestingly, in the same study it was found that mutation of the TTG2 (Transparent Testa Glabrous 2) gene, which results in reduction of integument cell elongation, also reduces endosperm growth (6). The TTG2 gene encodes a WRKY transcription factor, previously shown to be required for pigmentation of the seed coat as well as formation of