Parent-of-Origin Effects on Seed Size Modify Heterosis Responses in Arabidopsis thaliana

Abstract

Parent-of-origin effects arise when a phenotype depends on whether it is inherited maternally or paternally. Parent-of-origin effects can exert a strong influence on F1 seed size in flowering plants, an important agronomic and life-history trait that can contribute to biomass heterosis. Here we investigate the natural variation in the relative contributions of the maternal and paternal genomes to F1 seed size across 71 reciprocal pairs of F1 hybrid diploids and the parental effect on F1 seed size heterosis. We demonstrate that the paternally derived genome influences F1 seed size more significantly than previously appreciated. We further demonstrate (by disruption of parental genome dosage balance in F1 triploid seeds) that hybridity acts as an enhancer of genome dosage effects on F1 seed size, beyond that observed from hybridity or genome dosage effects on their own. Our findings indicate that interactions between genetic hybridity and parental genome dosage can enhance heterosis effects in plants, opening new avenues for boosting heterosis breeding in crop plants.

Keywords: Arabidopsis; Parent-of-origin effects; heterosis; hybridity; parental genome dosage; paternal contribution; ploidy; seed size.

FIGURE 1

Heterosis effects on F1 seed size observed in reciprocal F1 hybrid diploid seeds depends on parent-of-origin effects. (A) F1 hybrid diploid seed size of reciprocal crosses using 2x Ler-0 as pollen donor (represented by blue circles) or as maternal parent (light blue squares). Seed size of selfed isogenic parental lines is also represented (orange triangles) for comparison with their reciprocal F1 offspring. The horizontal red dashed line corresponds to the mean seed size value of the accession 2x Ler-0 (0.1332 mm²). Error bars represent SD. N ≥ 40 seeds/genotype. (B) Natural variation for parent-of-origin effects on seed size across 71 reciprocal F1 hybrid diploids. The red dashed line represents the average difference in mean F1 seed area for the entire set of 71 reciprocal hybrids.

FIGURE 2

Seed size phenotypes of reciprocal F1 hybrid diploid seeds and their parental lines. (A) The three F1 hybrid diploids with the weakest parent-of-origin effects on F1 seed size in this study and the accessions used as parental lines. The black arrow represents the intensity of parent-of-origin effects in ascending order. (B) The three F1 hybrid diploids with the strongest parent-of-origin effects in this study and their parental lines. The black arrow represents the intensity of parent-of-origin effects, from lowest to highest. Scale bar = 1 mm.

FIGURE 3

The heterotic effect on F1 diploid seed size depends on parent-of-origin effects. (A) Levels of Best-Parent (%BPH), Mid-Parent (%MPH) and Worst-Parent Heterosis (%WPH) across reciprocal F1 hybrid diploid seed size. (B) F1 hybrids that do not follow the trend observed among 71 reciprocal Ler-0/Accession F1 hybrids for %BPH, %MPH or %WPH. Exceptions are indicated in red. The horizontal dotted line represents the critical value 0.

FIGURE 4

Hybridity enhances parent-of-origin effects in F1 triploids beyond that achieved at the diploid level. (A) Difference in F1 mean seed size for reciprocal isogenic (Ler-0) and hybrid crosses at the diploid and triploid level. The red dashed line represents the parent-of-origin effects for Ler-0 F1 isogenic triploids. (B) F1 hybrid seed size of balanced-ploidy crosses (2x Accession X 2x Ler-0 and 2x Ler-0 X 2x Accession) and inter-ploidy crosses (2x Accession X 4x Ler-0 and 4x Ler-0 X 2x Accession). Seed size of parental lines is also represented (orange for the natural accessions, a horizontal red dashed line for 2x Ler-0 and black dashed line for 4x Ler-0) for comparison with ploidy levels and their reciprocal F1 offspring. Error bars represent SD. (C) Seed size phenotypes of reciprocal F1 seeds in balanced and inter-ploidy crosses. Scale bar = 1mm.

FIGURE 5

Hybridity has a greater effect on F1 seed size heterosis at the triploid level (3x). Mid-Parent Heterosis (MPH) levels in F1 3x seeds from reciprocal inter-ploidy crosses are shown. 2xA X 4xL (2x Accession X 4x Ler-0), 4xL X 2xA (4x Ler-0 X 2x Accession). The proportion due to hybridity is highlighted in yellow and it was calculated by subtracting the %MPH of reciprocal Ler-0 F1 isogenic inter-ploidy crosses (18.4% for 2x4 crosses, represented by a horizontal red dashed line, and –35.7% for 4x2 crosses, represented by a horizontal black dashed line) from the MPH levels of F1 hybrid triploids.