Plant biology

Turning fields into grains

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Cereal seeds contain an embryo and an endosperm, which is used as a food source. Differentiation of the endosperm is guided by several 'positional' molecular cues throughout development.

Which food supplies some 60% or more of the calories in the human diet? The answer is cereal plants — specifically, the endosperm of cereal seeds. The endosperm is a simple, nutrient- supplying tissue that surrounds the embryo of higher plants, and is composed of two types of cell: the protein- and oil-rich outer cells, and the starchy inner cells.

Writing in Development, Becraft and Asuncion-Crabb1 shed light on the factors involved in the development of these cell types. It used to be assumed that the characteristics of the cells are fixed two to three days after pollination. But, by re-examining genetic mosaics in the endosperm, Becraft and Asuncion-Crabb show that the fate of these cells can be changed at least up until the last cell division, as late as 22 days after pollination. The authors also identify three classes of 'kernel mosaic mutant', which correspond to three stages in the differentiation of the outer cells. The results might one day help in the manipulation of the oil, protein and carbohydrate content of cereal grains.

As plant cells are usually surrounded by rigid cell walls, there is little scope for them to migrate. So the shape and structure of plant organs is determined by the number of cell divisions and the extent of cell elongation. Similarly the specialization, or differentiation, of cells to perform different functions within a plant incorporates two types of event. For clonal events, the identity of a newly generated cell is determined by that of its parent. For position-dependent events, the identity of a cell is controlled by its position within an organ. Typically, clonal events are common early in development, occurring in meristems — the clusters of undifferentiated cells that spawn the developing organs. Positional events occur later, and can involve the switching of cells between different fates. Both clonal and positional effects come into play in the endosperm, and Becraft and Asuncion-Crabb1 flesh out the bones of our knowledge of the positional effects.

The endosperm, a major component of the cereal grain, originates from a fertilization event (of the maternal 'central' cell by a paternal sperm cell) that occurs in parallel to that which produces the embryo. The cereal endosperm consists of two basic cell types. The inner, energy-storage tissue is composed of starchy endosperm cells. These are surrounded by one to three layers of aleurone cells — protein- and oil-rich cells that secrete enzymes, allowing the mobilization of endosperm reserves during seed germination.

The first step in the formation of these cell types is the division of nuclei arranged around the periphery of the 'endosperm sac'. Each nucleus gives rise to a starchy endosperm 'initial' and an aleurone initial2 (Fig. 1a, b, overleaf), from which the two cell types originate after further divisions (Fig. 1c). These latter divisions could be seen simply as a clonal process. Alternatively, the further development of the aleurone initials might require a signal or signals from the surrounding maternal tissue — a positional effect.

Figure 1: Deciding the fate of seed endosperm cells.
figure1

a, b, Endosperm 'initial cells' (a) divide to give rise to aleurone and starchy endosperm initials (b; for simplicity, only one of each is shown). The initials then divide further, perpendicular to each other. c, The resulting cells differentiate to form aleurone and starchy endosperm cells. Becraft and Asuncion-Crabb1 show that positional cues are required to specify aleurone cells. Loss of function of the Dek1 gene leads to the conversion of aleurone cells to starchy endosperm cells. When gene function is restored, the outermost endosperm cells revert to aleurone cells. So the fate of an aleurone cell is not fixed; positional cues are required, and Dek1 responds to these cues. d, Becraft and Asuncion-Crabb also identified three broad categories of mutant maize plant, in which different stages of aleurone-cell differentiation are affected. The authors propose a three-stage differentiation process. Stage 1, the identity of the aleurone cell is controlled by its position within a gradient — from the seed's 'silk scar' to its 'abgerminal crown' — of the factor(s) affected in the first category of mutant plant. Stage 2, a few large fields of cells form, and cell fate is determined by position within those fields. Stage 3, many smaller fields form. Purple, endosperm; green, embryo. d is modified with permission from ref. 1.

Unusually, the endosperm is seen as an 'end-cell' system, in that it is not viable after the seed matures. Trying to persuade endosperm cells to divide further in tissue culture leads to a loss of the differentiated states of the two cell types. These observations suggest that endosperm cells are not plastic, that is, they cannot switch their fate. But Becraft and Asuncion-Crabb1 now show that this is not the case.

Using a common technique for inducing chromosome breaks, the authors eliminated the function of a gene called Dek1 in particular sectors in maize plants. In the resulting genetic mosaics, aleurone cells assumed the identity of starchy endosperm cells (Fig. 1c). The authors were then able to restore both Dek1 function and aleurone-cell identity to peripheral starchy endosperm cells in the affected sectors. As well as showing that cell fate is not fixed until late in endosperm development, these results reveal that the Dek1 gene is required to respond to positional cues that send early aleurone cells further down the road to specialization.

Becraft and Asuncion-Crabb went on to reveal further positional effects that fix the identity, and control the further differentiation, of aleurone cells. The authors looked at a variety of maize 'kernel mosaic' mutants that had regions in which the development of aleurone cells was abnormal. They then determined the extent of differentiation in the mutant sectors, and suggest that each of the mutant genes acts in one of three successive developmental stages (Fig. 1d).

In stage 1, an aleurone cell's identity is controlled by its position in a gradient, of unknown composition, across the inner part of the seed; this gradient is disrupted in stage-1 mutants. In stage 2, the further differentiation of an aleurone cell is determined by its position in relatively few large fields throughout the endosperm. During stage 3, the fate-determining fields are smaller and more numerous. The origin and nature of these developmental fields is not yet known: they may reflect cell groups connected by plasmodesmata (threads of cytoplasm), or they might originate from limiting dilution of some component(s) from either the sperm cell or the central cell.

The layer of developing starchy endosperm cells contains several discrete domains — with different biochemical properties and functions — that are characterized by their expression of particular 'marker' proteins3,4. One domain, the 'basal transfer layer', corresponds to a region specialized to promote solute uptake into the seed. The function of the second cellular domain, the embryo-surrounding region, is not yet clear3,4. We know little about whether or how these cell types can switch fates. But if they could be experimentally induced to change their destinies, the potential for changing the composition of the seed to suit the dietary needs of humans would be considerable. Likewise, one spin-off of Becraft and Asuncion-Crabb's1 findings might be a better ability to alter the proportion of protein- and oil-rich aleurone cells and starchy endosperm cells in the cereal grain.

References

  1. 1

    Becraft, P. W. & Asuncion-Crabb, Y. Development 127 , 4039–4048 (2000).

  2. 2

    Olsen, O.-A., Lemmon, B. & Brown, R. Trends Plant Sci. 3, 168– 169 (1998).

  3. 3

    Hueros, G., Varotto, S., Salamini, F. & Thompson, R. D. Plant Cell 7, 747–757 ( 1995).

  4. 4

    Opsahl-Ferstad, H.-G., Le Deunff, E., Dumas, C. & Rogowsky, P. M. Plant J. 12, 235–246 (1997).

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Correspondence to Richard D. Thompson.

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