Dynamics of maternal and paternal effects on embryo and seed development in wild radish (Raphanus sativus)

Abstract

Background and aims: Variability in embryo development can influence the rate of seed maturation and seed size, which may have an impact on offspring fitness. While it is expected that embryo development will be under maternal control, more controversial hypotheses suggest that the pollen donor and the embryo itself may influence development. These latter possibilities are, however, poorly studied. Characteristics of 10-d-old embryos and seeds of wild radish (Raphanus sativus) were examined to address: (a) the effects of maternal plant and pollen donor on development; (b) the effects of earlier reproductive events (pollen tube growth and fertilization) on embryos and seeds, and the influence of embryo size on mature seed mass; (c) the effect of water stress on embryos and seeds; (d) the effect of stress on correlations of embryo and seed characteristics with earlier and later reproductive events and stages; and (e) changes in maternal and paternal effects on embryo and seed characteristics during development.

Methods: Eight maternal plants (two each from four families) and four pollen donors were crossed and developing gynoecia were collected at 10 d post-pollination. Half of the maternal plants experienced water stress. Characteristics of embryos and seeds were summarized and also compared with earlier and later developmental stages.

Key results: In addition to the expected effects of the maternal plants, all embryo characters differed among pollen donors. Paternal effects varied over time, suggesting that there are windows of opportunity for pollen donors to influence embryo development. Water-stress treatment altered embryo characteristics; embryos were smaller and less developed. In addition, correlations of embryo characteristics with earlier and later stages changed dramatically with water stress.

Conclusions: The expected maternal effects on embryo development were observed, but there was also evidence for an early paternal role. The relative effects of these controls may change over time. Thus, there may be times in development when selection on the maternal, paternal or embryo contributions to development are more and less likely.

Fig. 1.

Proportion of 10-d embryos in each developmental stage for each pollen donor. Statistical analysis in Table 1.

Fig. 2.

Correlation coefficients for 10-d embryo and seed measurements with measurements of earlier and later development across all treatments. Fertilization is a composite measure of 12–24 h fertilization dynamics. * indicates significance at the 0·05 level.

Fig. 3.

Correlation coefficients for 10-d embryo and seed variables with earlier and later events by watering treatment. Shaded bars represent control treatment, while overlapping white and grey striped bars represent the water-stress treatments. ‘c’ indicates significance at the 0·05 level for control treatments, while ‘s’ indicates significance at the 0·05 level for stress treatments.

Fig. 4.

Percentage of 10-d embryos in four developmental stages on control and water-stressed plants. Statistics in Table 1.

Fig. 5.

Variance explained by pollen donor and maternal family for features of pollination, fertilization and embryo/seed development. Data for pollen germination, pollen tube length, fertilization, seed area at 3 d and final seed mass are from Marshall and Diggle (2001).