Programmed cell death (PCD): an essential process of cereal seed development and germination

Abstract

The life cycle of cereal seeds can be divided into two phases, development and germination, separated by a quiescent period. Seed development and germination require the growth and differentiation of new tissues, but also the ordered disappearance of cells, which takes place by a process of programmed cell death (PCD). For this reason, cereal seeds have become excellent model systems for the study of developmental PCD in plants. At early stages of seed development, maternal tissues such as the nucellus, the pericarp, and the nucellar projections undergo a progressive degeneration by PCD, which allows the remobilization of their cellular contents for nourishing new filial tissues such as the embryo and the endosperm. At a later stage, during seed maturation, the endosperm undergoes PCD, but these cells remain intact in the mature grain and their contents will not be remobilized until germination. Thus, the only tissues that remain alive when seed development is completed are the embryo axis, the scutellum and the aleurone layer. In germinating seeds, both the scutellum and the aleurone layer play essential roles in producing the hydrolytic enzymes for the mobilization of the storage compounds of the starchy endosperm, which serve to support early seedling growth. Once this function is completed, scutellum and aleurone cells undergo PCD; their contents being used to support the growth of the germinated embryo. PCD occurs with tightly controlled spatial-temporal patterns allowing coordinated fluxes of nutrients between the different seed tissues. In this review, we will summarize the current knowledge of the tissues undergoing PCD in developing and germinating cereal seeds, focussing on the biochemical features of the process. The effect of hormones and redox regulation on PCD control will be discussed.

Keywords: cereal; development; germination; plant; programmed cell death; seed.

FIGURE 1

Tissues undergoing PCD in developing and germinating cereal seeds. The upper panel represents the increase in seed length and storage accumulation taking as models the wheat and barley seeds. The lower panel indicates the periods of seed development in which the tissues undergo PCD. Stages of development: I, early development; II, differentiation; III, maturation. ESC, embryo-surrounding cells; DPA, days post anthesis (development); DAI, days after imbibition (germination).

FIGURE 2

Sections of wheat seeds at 3 DPA (left) and 16 DPA (right) stained with toluidine blue. Note the different tissues and how they change between these stages of seed development. P, pericarp; OI, outer integument; II, inner integument; N, nucellus; NP, nucellar projections; A, aleurone; E, starchy endosperm; EC, endosperm cavity. Bars, 100 μm.

FIGURE 3

TUNEL assay showing maternal tissues undergoing PCD at early and late stages of wheat seed development. In seeds at 5 DPA, nuclei from the nucellus and the integuments showed TUNEL-positive signal. Note the reduction of pericarp width and the formation of seed cuticles as a consequence of PCD (compare 5 DPA vs 25 DPA). Starch granules of different sizes are also observed in the starchy endosperm. P, pericarp; OI, outer integument; II, inner integument; NE, nucellar epidermis; NP, nucellar parenchyma; OP, outer pericarp; IP, inner pericarp; I, pigmented cuticle derived from outer and inner integuments; A, aleurone; E, starchy endosperm. Bars, 50 μm.

FIGURE 4

Hormonal control of PCD in developing and germinating cereal seeds. Tissues undergoing PCD are represented in blue. Fluxes of nutrients promoted by PCD events are indicated by red arrows. Cells of the starchy endosperm undergo PCD during development but remain intact until germination. A, aleurone; E, endosperm; N, nucellus; NP, nucellar projections; P, pericarp; R, root; RAM, root apical meristem; S, shoot; SAM, shoot apical meristem; Sc, scutellum; ABA, abscisic acid; IAA, indol acetic acid; JA, jasmonic acid; GA, gibberellic acid; ROS, reactive oxygen species.